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Sex-Linked Transcription Factor Involved in a Shift of Sex-Pheromone Preference in the Silkmoth Bombyx Mori

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Sex-Linked Transcription Factor Involved in a Shift of Sex-Pheromone Preference in the Silkmoth Bombyx Mori Sex-linked transcription factor involved in a shift of sex-pheromone preference in the silkmoth Bombyx mori Tsuguru Fujiia, Takeshi Fujiib, Shigehiro Namikic, Hiroaki Abed, Takeshi Sakuraic, Akio Ohnumae, Ryohei Kanzakic, Susumu Katsumaa, Yukio Ishikawab, and Toru Shimadaa,1 aLaboratory of Insect Genetics and Bioscience, Department of Agricultural and Environmental Biology, University of Tokyo, Tokyo 113-8657, Japan; bLaboratory of Applied Entomology, Department of Agricultural and Environmental Biology, University of Tokyo, Tokyo 113-8657, Japan; cResearch Center for Advanced Science and Technology, University of Tokyo, Tokyo 153-8904, Japan; dLaboratory of Insect Functional Biochemistry, Department of Biological Production, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan; and eInstitute of Sericulture, Ami, Ibaraki 300-0324, Japan Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved September 26, 2011 (received for review June 9, 2011) In the sex-pheromone communication systems of moths, odorant The silkmoth Bombyx mori has been used as a model for receptor (Or) specificity as well as higher olfactory information studying sex-pheromone communication systems in moths. B. mori processing in males should be finely tuned to the pheromone of females secrete an ∼11:1 mixture of bombykol [(E,Z)-10,12- conspecific females. Accordingly, male sex-pheromone preference hexadecadien-1-ol] and bombykal [(E,Z)-10,12-hexadecadien- should have diversified along with the diversification of female 1-al] from the pheromone gland (14). Bombykol alone elicits sex pheromones; however, the genetic mechanisms that facili- full courtship behavior in males, whereas bombykal alone shows tated the diversification of male preference are not well un- no apparent activity (14). Odorant receptors (Ors) for bombykol derstood. Here, we explored the mechanisms involved in a drastic (BmOr1) and bombykal (BmOr3) are pheromone receptors shift in sex-pheromone preference in the silkmoth Bombyx mori identified in Lepidoptera (7, 8). The genes encoding these Ors using spli mutants in which the genomic structure of the gene reside on the Z chromosome (7–9). The Ors are expressed in Bmacj6, which encodes a class IV POU domain transcription factor, two specialized chemosensory neurons in the long sensilla tri- is disrupted or its expression is repressed. B. mori females secrete chodea on the male antenna (8). Olfactory receptor neurons an ∼11:1 mixture of bombykol and bombykal. Bombykol alone (ORNs) responding to bombykol and bombykal project to the elicits full male courtship behavior, whereas bombykal alone macroglomerular complex (MGC) in the brain of male moths, shows no apparent activity. In the spli mutants, the behavioral where the information on pheromone reception is integrated responsiveness of males to bombykol was markedly reduced, (15). The MGC of B. mori consists of three subdivisions: the whereas bombykal alone evoked full courtship behavior. The re- toroid, cumulus, and horseshoe. ORNs responding to bombykol duced response of spli males to bombykol was explained by the and bombykal send their axons to the toroid and cumulus, re- paucity of bombykol receptors on the male antennae. It was also spectively (16). found that, in the spli males, neurons projecting into the toroid, A large variety of mutants are available in B. mori, repre- a compartment in the brain where bombykol receptor neurons senting all major stages of development (the egg, larva, pupa, normally project, responded strongly to bombykal. The present and adult) (17). The availability of complete genome data for B. study highlights a POU domain transcription factor, Bmacj6, which mori (18–20) combined with these mutants provides unparalleled may have caused a shift of sex-pheromone preference in B. mori opportunities to isolate and analyze the genes governing bi- Or through gene choice and/or axon targeting. ologically important traits in Lepidoptera. To date, genes re- sponsible for over 20 mutants have been identified by positional Z chromosome | olfactory receptor | atavism | speciation | food preference cloning or candidate gene approaches (21). The Z-chromosome–linked mutant spli is characterized by a oths possess highly diverse and complex sex-pheromone soft and pliable larval body. We previously reported that (i)a Mcommunication systems. A combination of compounds and 66- to 96-kb sequence is deleted from the Z chromosome in the fine blending confer high species specificity, crucial to the re- spli mutant and that (ii) only Bmacj6,aDrosophila acj6 homolog productive isolation of moths (1, 2). To date, great efforts have encoding a class IV POU domain transcription factor, is com- been made to clarify the genes responsible for generating pher- putationally predicted in the deleted sequence (22). We con- omone diversity by using pheromone strains within a species or cluded that disruption of Bmacj6 is associated with the spli closely related species. Recently, it was shown that allelic vari- phenotype (22). Subsequently, analysis with full-length cloning of ation in the fatty-acyl reductase gene or selective transcription of Bmacj6 has clarified that, among the four exons of the gene, desaturase genes is responsible for female sex-pheromone varia- exons 2–4, which encode a POU domain, are missing in the spli tion in the moth genus Ostrinia (3–5). In contrast to the progress mutant (Fig. S1). In Drosophila, acj6 mutants exhibit abnormal made in understanding the genes responsible for diversification of pheromone production, the molecular mechanisms that shift sex- pheromone preferences in male moths are not well understood. Author contributions: Tsuguru Fujii, Takeshi Fujii, S.N., H.A., A.O., R.K., S.K., Y.I., and An interesting genetic feature of sex-pheromone preference in T. Shimada designed research; Tsuguru Fujii, Takeshi Fujii, S.N., and T. Sakurai performed research; Tsuguru Fujii, Takeshi Fujii, S.N., and Y.I. analyzed data; and Tsuguru Fujii, moths is its sex linkage. In most moths, the sex chromosome’s Takeshi Fujii, S.N., and Y.I. wrote the paper. constitution is Z/W in females and Z/Z in males (6). Some of the The authors declare no conflict of interest. genes encoding sex-pheromone receptors, which are important This article is a PNAS Direct Submission. factors determining the preference of the males, are reported to Data deposition: The sequences reported in this paper have been deposited in the be Z-linked in Bombyx (7–9), Heliothis (10), and Ostrinia (9, 11). GenBank database (accession nos. AB623137–AB623142 and AB635375–AB635378). Ostrinia nubilalis 1 In , a shift in male behavioral responses in the To whom correspondence should be addressed. E-mail: [email protected]. Resp two pheromone strains is controlled by a locus called that This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. maps to the Z chromosome (12, 13). 1073/pnas.1107282108/-/DCSupplemental. 18038–18043 | PNAS | November 1, 2011 | vol. 108 | no. 44 www.pnas.org/cgi/doi/10.1073/pnas.1107282108 Downloaded by guest on September 26, 2021 olfactory behavior and reduced mobility (23–25), and genetic responses. When the male spli moths (spli/spli) and the male gray spli spli and electrophysiological analyses suggested that acj6 determines moths with a normal spli locus (+ /+ , mln/mln) were placed Or gene choice and axon targeting of ORNs (24, 26). around two vials releasing either bombykal or bombykol, the Here, we report that (i) the Bt mutant, originally characterized normal moths were specifically attracted to bombykol, whereas Bt by an abnormal feeding behavior, bears an allele of spli (spli ); the spli males were specifically attracted to bombykal (Movie S1). (ii) behavioral responsiveness of the male spli mutants (spli and These findings indicate that bombykal, rather than bombykol, Bt spli ) to bombykol is markedly reduced in association with the elicited courtship behavior in the spli mutants. paucity of bombykol receptors on the antennae; (iii) full court- ship behavior of spli males is evoked by bombykal alone; and (iv) Electrophysiological and Molecular Analysis of the spli Male neurons projecting into the toroid, a compartment in the brain Antennae. To elucidate the cause of the diminished behavioral spli where bombykol receptor neurons normally project, respond response of males to bombykol, we measured electroan- tennogram (EAG) responses of male spli moths to bombykol and to bombykal. Bt bombykal. Whereas the response of spli and spli males to Results bombykal was similar to the response of p50T (+/+) and spli/+ A fi Identification of a spli Allele. The Z-chromosome–linked mutant Bt males (Fig. 3 ), the response to bombykol was signi cantly re- spli is known for abnormal feeding on plants other than mulberry (27). duced compared with the response of p50T (+/+) and /+ A We noted that the larval body of this mutant was soft and pliable, males (Fig. 3 ). This result suggested that the expression of fi which are characteristics of the spli mutant. Crossing of Bt males the odorant receptor for bombykol (BmOr1) was speci cally spli (Bt/Bt) with normal females (+/W) and spli females (spli/W) sug- decreased in the mutants. To test this possibility, we de- BmOr1 BmOr3 gested that the Bt mutant bears an allele of spli,whichwedesig- termined the expression levels of and in the male Bt antenna by quantitative RT-PCR (qRT-PCR). Whereas expres- nated spli (Table S1). RT-PCR analysis of Bmacj6, disruption of Bt spli sion levels of BmOr3 in the spli and spli males were almost the which is associated with the phenotype (22) (Fig. S1), showed spli B that, in contrast to the expression in the nervous system and some same as those in p50T (+/+) and /+ males (Fig. 3 ), 354- and 1,085-fold reductions in BmOr1 expression were observed in other tissues in the normal strain, no expression was observed in Bt Bt spli spli B any tissues tested in the spli mutant (Fig.
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