Dataset Information

The Role of the Dopamine Melanin Pathway in the Ontogeny of Elytral Melanization in Harmonia axyridis.

ABSTRACT: Polymorphic melanism in insects is a conspicuous phenotype which is derived from specific genotypes, and might be central to speciation processes via assortative sexual selection. At the molecular level, melanism in insects is attributed to the melanin pathway. DOPA decarboxylase (DDC) protein encoded by the DDC gene plays a central role in dopamine-melanin synthesis, the main component of melanin in insects. Although the mechanism of melanism has been elucidated in holometabolous insects, other physiological processes coupled with melanin synthesis are unknown. Herein, we identified DDC from the Asian multi-colored ladybird (Harmonia axyridis), an ideal holometabolous insect for studies of melanization due to highly variable color on their elytra. Analyses revealed that HaDDC (the DDC gene of H. axyridis) was constitutively expressed throughout all developmental stages. We performed RNAi technique to examine the melanin synthesis pathway of elytra in H. axyridis. The transcript levels of HaDDC were significantly suppressed after the injection of double-strand RNA of HaDDC (dsHaDDC) at 300 ng/individual in third instar larvae. Silencing HaDDC in third instar larvae did not result in mortality nor significantly affect pupation and eclosion. We further demonstrated that all adults of H. axyridis (forms succinea, spectabilis, and conspicua) with HaDDC silenced in third larvae showed abnormal phenotype which emerged as decreased elytra melanin. However, melanin was still observed in other parts of the adults such as head or pronotum. These results demonstrate for the first time that dopamine-derived melanin is the main contributor in elytra melanization in H. axyridis. Additionally, we provide evidence for DDC in regulating fecundity by showing that silencing of HaDDC in third instar larvae significantly reduced female egg-laying and egg hatching. As such, DDC is likely pleiotropic in respect of its role in melanin production and fecundity processes. These findings bring novel insights into melanin production in holometabolous insects, and contribute to the framework on which further studies may be conducted on the mechanism of pigment production and patterning in various types of insect coloration.

SUBMITTER: Chen X

PROVIDER: S-EPMC6719567 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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The Role of the Dopamine Melanin Pathway in the Ontogeny of Elytral Melanization in <i>Harmonia axyridis</i>.

Chen Xu X Xiao Da D Du Xiaoyan X Guo Xiaojun X Zhang Fan F Desneux Nicolas N Zang Liansheng L Wang Su S

Frontiers in physiology 20190827

Polymorphic melanism in insects is a conspicuous phenotype which is derived from specific genotypes, and might be central to speciation processes via assortative sexual selection. At the molecular level, melanism in insects is attributed to the melanin pathway. DOPA decarboxylase (DDC) protein encoded by the <i>DDC</i> gene plays a central role in dopamine-melanin synthesis, the main component of melanin in insects. Although the mechanism of melanism has been elucidated in holometabolous insects ...[more]

PMID: 31507439

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Project description:The GATA transcription factor Pannier is identified as the major regulatory gene in color pattern formation in the Asian multi-colored ladybird beetle (Harmonia axyridis). however, the mechanisms of Pannier in regulating melanin synthesis and development in H. axyridis remain elusive. In this study, we identified and characterized Pannier in H. axyridis (HaPnr) and showed it to have two alternative spliced variants named HaPnr-α and HaPnr-β. Analyses of developmental stage expression patterns revealed that HaPnr, HaPnr-α and HaPnr-β were constitutively expressed throughout all developmental stages. To examine the role of HaPnr in H. axyridis development, RNA interference was performed in late larvae (the fourth instar) and early pupae (the first day of pupa stage). The transcript levels of HaPnr were effectively suppressed after the injection of double-stranded RNA of HaPnr (dsHaPnr). The fourth instar larvae injected with dsHaPnr reduced the pupation rates to only 61.50%, compared with 88.5% in the dsGFP-injected group. The un-pupated larvae gradually died after 1 week, and visually unaffected pupae emerged into abnormal adults with malformed hind wings and melanin absent from the cuticle. These abnormal adults gradually died 10 days after eclosion. However, when early pupae were injected with dsHaPnr, the normal eclosion rate was achieved at 88.41% on day 6 after the injection. In addition, these successful eclosion adults also showed an absence of melanin in the cuticle, but they could mate normally and have normal fecundity as compared with the control. We further demonstrated that the suppression of HaPnr-α or HaPnr-β individually did not affect the pupation and eclosion process. The suppression of HaPnr-α expression resulted in elytra melanin decreasing in both the conspicua and the succinea subgroup in H. axyridis. Even though the suppression of HaPnr-β expression only affected the melanin synthesis in the succinea subgroup, it significantly prolonged the time taken for melanin synthesis to occur in the conspicua subgroup in H. axyridis. These results indicate that HaPnr plays an essential role in insect development, especially during their metamorphosis, and also support our hypothesis that HaPnr could regulate melanin synthesis in H. axyridis under the combined action with its two splicing variants, HaPnr-α and HaPnr-β.

Project description:The ambient temperature experienced during development is a crucial factor affecting survival and adult phenotype in ectotherms. Moreover, the exact response of individuals to different temperature regimes is frequently sex-specific. This sex-specific response can result in varying levels of sexual dimorphism according to the experienced conditions. The majority of studies have investigated the effects of temperature on individuals reared under a constant temperature regime throughout their whole preimaginal development, whereas information on stage-dependent variation in temperature effects is scarce. Here we investigate how the stage at which elevated temperature is experienced influences survival, adult body size and colouration in the harlequin ladybird Harmonia axyridis form succinea. The effects of timing of exposure to elevated temperature on the adult phenotype are assessed separately for males and females. Control individuals were reared at a constant temperature of 20 °C. Beetles in other treatments were additionally exposed to 33 °C for 48 hours during the following developmental stages: egg, 1(st) to 2(nd) larval instar, 3(rd) larval instar, 4(th) larval instar and pupa. Exposure to an elevated temperature during the early developmental stages resulted in lower survival, but the adult phenotype of survivors was almost unaffected. Exposure to an elevated temperature during the later developmental stages (4(th) larval instar or pupa) resulted in the decreased melanisation of elytra, decreased structural body size and increased dry mass. Furthermore, the timing of high temperature exposure affected the degree of sexual dimorphism in elytral melanisation and dry mass. We demonstrate that the effects of elevated temperature can vary according to the developmental stage at exposure. Detailed information on how ambient temperature affects the developmental biology of ectotherms is crucial for modeling population growth and predicting the spread of invasive species such as Harmonia axyridis.

Dataset Information

The Role of the Dopamine Melanin Pathway in the Ontogeny of Elytral Melanization in Harmonia axyridis.

Publications

The Role of the Dopamine Melanin Pathway in the Ontogeny of Elytral Melanization in <i>Harmonia axyridis</i>.

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