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Pheromone gland development and monoterpenoid synthesis specific to oviparous females in the pea aphid.

ABSTRACT: Background:Aphids display "cyclic parthenogenesis," in which parthenogenetically and sexually reproducing morphs seasonally alternate in the aphid annual life cycles. There are various characteristics that differ between asexual viviparous and sexual oviparous females. In oviparous females, swollen cuticular structures (~?10 ?m in diameter), called "scent plaques," are scattered on the surface of hind tibias, and secrete monoterpenoid sex pheromones. However, the developmental processes of the pheromone glands and the biosynthetic pathways of monoterpenoid pheromones have yet to be elucidated. Results:Comparisons of the developmental processes that form hind tibias between sexual and parthenogenetic females revealed that, in sexual females, the epithelial tissues in proximal parts of hind tibias become columnar in fourth instar nymphs, and circular pheromone glands with Class 1 gland cells appear in adults, although they do not appear in parthenogenetic females. Furthermore, by comparing the expression levels of genes involved in the mevalonate pathway, which is required for monoterpenoid synthesis, we show that genes that encode the downstream enzymes in the pathway are highly expressed in hind tibias of sexual females. Conclusion:Glandular tissues of scent plaque are differentiated from the fourth instar in sexual females, while parthenogenetic females lack the glandular cells. Only the downstream steps of the mevalonate pathway appear to occur in scent plaques on hind tibias of sexual females, although the upstream steps may occur somewhere in other body parts.

SUBMITTER: Murano K

PROVIDER: S-EPMC5946545 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Pheromone gland development and monoterpenoid synthesis specific to oviparous females in the pea aphid.

Murano Koki K Ogawa Kota K Kaji Tomonari T Miura Toru T

Zoological letters 20180511

<h4>Background</h4>Aphids display "cyclic parthenogenesis," in which parthenogenetically and sexually reproducing morphs seasonally alternate in the aphid annual life cycles. There are various characteristics that differ between asexual viviparous and sexual oviparous females. In oviparous females, swollen cuticular structures (~ 10 μm in diameter), called "scent plaques," are scattered on the surface of hind tibias, and secrete monoterpenoid sex pheromones. However, the developmental processes ...[more]

PMID: 29780614

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Project description:BackgroundGermline specification in some animals is driven by the maternally inherited germ plasm during early embryogenesis (inheritance mode), whereas in others it is induced by signals from neighboring cells in mid or late development (induction mode). In the Metazoa, the induction mode appears as a more prevalent and ancestral condition; the inheritance mode is therefore derived. However, regarding germline specification in organisms with asexual and sexual reproduction it has not been clear whether both strategies are used, one for each reproductive phase, or if just one strategy is used for both phases. Previously we have demonstrated that specification of germ cells in the asexual viviparous pea aphid depends on a preformed germ plasm. In this study, we extended this work to investigate how germ cells were specified in the sexual oviparous embryos, aiming to understand whether or not developmental plasticity of germline specification exists in the pea aphid.ResultsWe employed Apvas1, a Drosophila vasa ortholog in the pea aphid, as a germline marker to examine whether germ plasm is preformed during oviparous development, as has already been seen in the viviparous embryos. During oogenesis, Apvas1 mRNA and ApVas1 protein were both evenly distributed. After fertilization, uniform expression of Apvas1 remained in the egg but posterior localization of ApVas1 occurred from the fifth nuclear cycle onward. Posterior co-localization of Apvas1/ApVas1 was first identified in the syncytial blastoderm undergoing cellularization, and later we could detect specific expression of Apvas1/ApVas1 in the morphologically identifiable germ cells of mature embryos. This suggests that Apvas1/ApVas1-positive cells are primordial germ cells and posterior localization of ApVas1 prior to cellularization positions the preformed germ plasm.ConclusionsWe conclude that both asexual and sexual pea aphids rely on the preformed germ plasm to specify germ cells and that developmental plasticity of germline specification, unlike axis patterning, occurs in neither of the two aphid reproductive phases. Consequently, the maternal inheritance mode implicated by a preformed germ plasm in the oviparous pea aphid becomes a non-canonical case in the Hemimetabola, where so far the zygotic induction mode prevails in most other studied insects.

Dataset Information

Pheromone gland development and monoterpenoid synthesis specific to oviparous females in the pea aphid.

Publications

Pheromone gland development and monoterpenoid synthesis specific to oviparous females in the pea aphid.

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