Juvenile hormone regulates the photoperiodic plasticity of elytra coloration in a ladybird Harmonia axyridis

Authors: LI, JIA-XU - Huazhong Agricultural University; TIAN, ZHONG - Huazhong Agricultural University; LIU, XING-FENG - Huazhong Agricultural University; LI, BEI - Huazhong Agricultural University; AN, HOA-MIN - Huazhong Agricultural University; Brent, Colin; WANG, JIA-LU - Huazhong Agricultural University; WANG, XIAO-PING - Huazhong Agricultural University; LIU, WEN - (NCE, CECR)networks Of Centres Of Exellence Of Canada, Centres Of Excellence For Commercilization A

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/20/2023
Publication Date: 5/22/2023
Citation: Li, J., Tian, Z., Liu, X., Li, B., An, H., Brent, C.S., Wang, J., Wang, X., Liu, W. 2023. Juvenile hormone regulates the photoperiodic plasticity of elytra coloration in a ladybird Harmonia axyridis. Molecular Ecology. 32:2884-2897. https://doi.org/10.1111/mec.16896.
DOI: https://doi.org/10.1111/mec.16896

Interpretive Summary: Many animals, including insects, exhibit variable body color in response to environmental challenges. Changes to pigments in the cuticle facilitate this body color flexibility, however, the mechanisms by which environmental cues regulate pigment expression remain largely unknown. In this study, we used the ladybird Harmonia axyridis as a model to investigate changes in the color of the outer wings, the elytra, in response to varied daylength, and its endocrine regulation. It was found that females under long-day conditions develop elytra that are much redder than those under short-day conditions, resulting from the differential accumulation of pigments. Hormone application and RNAi-mediated gene knockdown indicate that pigment transport was directed by a gene expression pathway that is responsive to levels of juvenile hormone (JH), which also controls egg production. We identified several genes that were crucial to this response.

Technical Abstract: Many animals, including insects, exhibit plasticity of body color in response to environmental challenges. Varied expression of carotenoids, major cuticle pigments, significantly contributes to body color flexibility. However, the molecular mechanisms by which environmental cues regulate carotenoid expression remain largely unknown. In this study, we used the ladybird Harmonia axyridis as a model to investigate photoperiodic-responsive plasticity of elytra coloration and its endocrine regulation. It was found that H. axyridis females under long-day conditions develop elytra that are much redder than those under short-day conditions, resulting from the differential accumulation of carotenoids. Exogenous hormone application and RNAi-mediated gene knockdown indicate that carotenoid deposition was directed through the juvenile hormone (JH)receptor-mediated canonical pathway. Moreover, we characterized an SR-BI/CD36 (SCRB) gene SCRB10 as the carotenoid transporter responding to JH signaling and regulating the elytra coloration plasticity. Taken together, we propose that JH signaling transcriptionally regulates the carotenoid transporter gene for photoperiodic coloration plasticity of elytra in the beetles, which reveals a novel role of the endocrine system in the regulation of carotenoid-associated animal body coloration under environmental stimuli.