Alternative suppression of transcription from two desaturase genes is the key for species-specific sex pheromone biosynthesis in two Ostrinia moths

Sakai, Ryota; Fukuzawa, Mai; Nakano, Ryo; Tatsuki, Sadahiro; Ishikawa, Yukio

doi:10.1016/j.ibmb.2008.10.001

Cited by 37 publications

(38 citation statements)

References 29 publications

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“…The composition of available acyl precursors may differ from species to species, which in itself contributes to variation in blend composition (26). Indeed, differential regulation of desaturase genes has been shown to be associated with evolutionary transitions in the pheromone communication systems of flies and moths including in Ostrinia (9,11,(28)(29)(30)(31). However, in most Ostrinia species, the precursor and pheromone component ratios exhibit significant disparities, and the pgFAR substrate preference is in many cases necessary to explain how the final blend ratios are obtained.…”

Section: Discussionmentioning

confidence: 99%

Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths

Lassance

Liénard

Antony

et al. 2013

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

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Pheromones are central to the mating systems of a wide range of organisms, and reproductive isolation between closely related species is often achieved by subtle differences in pheromone composition. In insects and moths in particular, the use of structurally similar components in different blend ratios is usually sufficient to impede gene flow between taxa. To date, the genetic changes associated with variation and divergence in pheromone signals remain largely unknown. Using the emerging model system Ostrinia, we show the functional consequences of mutations in the protein-coding region of the pheromone biosynthetic fatty-acyl reductase gene pgFAR. Heterologous expression confirmed that pgFAR orthologs encode enzymes exhibiting different substrate specificities that are the direct consequences of extensive nonsynonymous substitutions. When taking natural ratios of pheromone precursors into account, our data reveal that pgFAR substrate preference provides a good explanation of how species-specific ratios of pheromone components are obtained among Ostrinia species. Moreover, our data indicate that positive selection may have promoted the observed accumulation of nonsynonymous amino acid substitutions. Site-directed mutagenesis experiments substantiate the idea that amino acid polymorphisms underlie subtle or drastic changes in pgFAR substrate preference. Altogether, this study identifies the reduction step as a potential source of variation in pheromone signals in the moth genus Ostrinia and suggests that selection acting on particular mutations provides a mechanism allowing pheromone reductases to evolve new functional properties that may contribute to variation in the composition of pheromone signals.

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Section: Discussionmentioning

confidence: 99%

Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths

Lassance

Liénard

Antony

et al. 2013

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

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“…Alternatively, the simultaneous production of E and Z isomers may be a derivative trait. This mutation might have contributed to the diversification of sex pheromone components in Ostrinia together with the advent of fatty acid reductases varying in substrate specificity (7,14,21,22). At present, we do not know which scenario is correct, but the expression of pheromone receptors specific for E11-14:OH in the male antennae of all Ostrinia species examined to date (23) seems to support the latter scenario.…”

Section: Discussionmentioning

confidence: 94%

Sex pheromone desaturase functioning in a primitive Ostrinia moth is cryptically conserved in congeners’ genomes

Fujii

Ito

Tatematsu

et al. 2011

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

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(E)-11-and (Z)-11-tetradecenyl acetate are the most common female sex pheromone components in Ostrinia moths. The Δ11-desaturase expressed in the pheromone gland (PG) of female moths is a key enzyme that introduces a double bond into pheromone molecules. A single Δ11-desaturase of Ostrinia nubilalis, OnubZ/ E11, has been shown to produce an ∼7:3 mixture of (E)-11-and (Z)-11-tetradecenoate from the substrate tetradecanoate. In contrast, the sex pheromone of Ostrinia latipennis, a primitive species of Ostrinia, is (E)-11-tetradecenol. This pheromone is unique in that it is not acetylated, and includes no Z isomer. In the present study, through the cloning and functional analysis of a PG-specific Δ11-desaturase in O. latipennis, we showed that the absence of the Z isomer in the pheromone is attributable to the strict product specificity of the Δ11-desaturase in this species, LATPG1. Phylogenetic analysis revealed that LATPG1 was not closely related to OnubZ/ E11. Rather, it was closely related to retroposon-linked cryptic Δ11-desaturases (ezi-Δ11) found in the genomes of O. nubilalis and Ostrinia furnacalis. Taken together, the results showed that an unusual Δ11-desaturase is functionally expressed in O. latipennis, although the genes encoding this enzyme appear to be cryptic in congeners.baculovirus expression system | speciation M ost moths use a mate-finding system that involves the longdistance attraction of males with female sex pheromones (1). The great majority of moth pheromones are a blend of unsaturated C 10 -C 18 primary acetates, alcohols, or aldehydes, and the combination of components and the blend ratios confer high species specificity to the signal (1). Given the primary role of sex pheromones in reproductive behavior, the divergence of pheromone signals should have profoundly affected premating reproductive isolation and speciation in moths (for a review, see ref.2). Moths of the genus Ostrinia (Lepidoptera: Crambidae), which show distinct differences in sex pheromones (3), are useful for studying the evolution of sex pheromone communication systems. The European corn borer Ostrinia nubilalis has long been a model for studies on this subject (4-7). Given the wealth of information available on the genetic, biochemical, and molecular aspects of sex pheromone production and reception in this species, comparative studies using congeners should shed new light on the subject. Among the 21 species of Ostrinia recorded worldwide (4, 8), the sex pheromones of nine species, including O. nubilalis, have been characterized to date (8,9). (E)-11-and (Z)-11-tetradecenyl acetate (E11-and Z11-14:OAc) are the most common female sex pheromone components in Ostrinia (10). The sex pheromone components in Ostrinia are produced de novo in the pheromone gland (PG) of female moths from a common fatty acid, palmitic acid, through several enzymatic reactions (i.e., limited β oxidation, desaturation, reduction, and acetylation) (11)(12)(13)(14). A desaturase specifically expressed in the PG is the key enzyme that introduces ...

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“…Sex pheromones secreted by Ostrinia moths are blends of monounsaturated tetradecenyl (C 14 ) acetates, which differ in the position of the double bond (9, 11, or 12) and its geometry (Z or E). In Ostrinia nubilalis and Ostrinia scapulalis, the Z-and E-isomers of the double bond are produced by a single D11-desaturase (Fukuzawa et al, 2006;Roelofs et al, 2002;Sakai et al, 2009;Xue et al, 2007), which we have referred to as 'Z/ED11' in this study. On the other hand, only the E-isomer is produced by the D11-desaturase expressed in the pheromone gland of Ostrinia latipennis, LATPG1(¼ED11) (Fujii et al, 2011).…”

Section: Introductionmentioning

confidence: 93%

“…Moths belonging to the genus Ostrinia (Lepidoptera: Crambidae) are good models for understanding the genetic bases of the evolution of moth sex pheromones (Fujii et al, 2011;Knipple et al, 2002;Lassance et al, 2010;Roelofs et al, 2002;Roelofs and Rooney, 2003;Rooney, 2011;Sakai et al, 2009;Xue et al, 2007). Sex pheromones secreted by Ostrinia moths are blends of monounsaturated tetradecenyl (C 14 ) acetates, which differ in the position of the double bond (9, 11, or 12) and its geometry (Z or E).…”

Section: Introductionmentioning

confidence: 99%

Multiple Δ11-desaturase genes selectively used for sex pheromone biosynthesis are conserved in Ostrinia moth genomes

Fujii

Yasukochi

Rong

et al. 2015

Insect Biochemistry and Molecular Biology

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Alternative suppression of transcription from two desaturase genes is the key for species-specific sex pheromone biosynthesis in two Ostrinia moths

Cited by 37 publications

References 29 publications

Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths

Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths

Sex pheromone desaturase functioning in a primitive Ostrinia moth is cryptically conserved in congeners’ genomes

Multiple Δ11-desaturase genes selectively used for sex pheromone biosynthesis are conserved in Ostrinia moth genomes

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