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Interruption of the juvenile hormone signaling pathway affects oocyte maturation in Apis mellifera queens

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Author(s):
Thiago da Silva Depintor
Total Authors: 1
Document type: Doctoral Thesis
Press: Ribeirão Preto.
Institution: Universidade de São Paulo (USP). Faculdade de Medicina de Ribeirão Preto (PCARP/BC)
Defense date:
Examining board members:
Zila Luz Paulino Simoes; Fábio Camargo Abdalla; David de Jong; José Eduardo Serrão
Advisor: Zila Luz Paulino Simoes
Abstract

During insect development, networks of gene interaction are activated in response to two morphogenetic hormones: juvenile hormone (JH) and 20-hydroxyecdysone (20E). The activation of these networks is responsible for morphological and physiological changes that characterize the developmental stages: egg (embryo), larva, pupa, and adult. JH binds to nuclear receptors, notably methoprene tolerant (MET), forming a complex that promotes the transcription of other transcription factors, such as Krüppel homolog 1 (Kr-h1), which prevents premature molting during development. JH is at the top of the hierarchy controlling these networks; however, it is known that environmental factors influence the levels of circulating hormones. In Apis mellifera, our model organism, female larvae can develop in two different nutritional environments, resulting in two distinct castes, queens and workers. These castes are physiologically different; for example, queens have up to 20 times more JH at a specific stage of development compared to workers. In this study, we analysed the expression profile of JH response genes, Met, ET, Tai, and E93, during the developmental stages of queens and workers. We found that during pre-imaginal development, Met shows expression peaks when the levels of circulating JH in the hemolymph are undetectable. We also demonstrated that the Met gene in workers responds differently to hormonal stimulation (JH III) depending on the developmental stage. Using systemic RNAi, we showed that silencing Met in the pupal stages of workers does not alter the expression of Kr-h1, an important component in the JH pathway, but alters the expression of E93, a key component of the 20E pathway, suggesting that Met has a role outside the JH signaling pathway, specifically in the 20E pathway during the studied stages. In adult queens, we silenced Met and a key enzyme in the JH biosynthesis, juvenile hormone acid methyltransferase (jhamt). We observed that silencing Met alters oocyte maturation during the first days of a queen\'s life, particularly affecting the number of active ovarioles and the size of the basal ovarian follicle. The groups treated with dsjhamt also confirmed these results by inducing similar phenotypes. Our results show that JH plays a role in the maturation of oocytes during the first days after adult emergence. Additionally, they suggest that the ovaries might be a secondary source of JH. This study contributes to a better understanding of the JH-triggered signaling pathway during pre-imaginal development and its relationship with oocyte maturation mediated by the intracellular receptor MET during the early days of an adult queen\'s life. (AU)

FAPESP's process: 20/04166-4 - Activation of complexes gene network of interactions in response to modulation by endogenous and environmental factors during development of workers and queens of Apis mellifera
Grantee:Thiago da Silva Depintor
Support Opportunities: Scholarships in Brazil - Doctorate