Role of juvenile hormone receptor Methoprene-tolerant 1 in silkworm larval brain development and domestication.

Yong Cui,华南师范大学生命科学学院昆虫科学与技术研究所，广东省昆虫发育生物学与应用技术重点实验室，广州市昆虫发育调控与应用研究重点实验室，广东 广州 510631，中国 ,Cen-Cen Li,Lang You,中国科学院上海生物科学研究所植物生理生态研究所，中国科学院昆虫发育与进化生物学重点实验室，上海 200032，中国 ,Hui-Min Deng, ,Zi-Dan Zhu,Yong-Ping Huang,信阳师范学院生命科学学院，河南 信阳 464000，中国 ,Xiang-Min Wei,Zu-Lian Liu,Hui Xiang,Yong-Jian Lin,Qi-Li Feng

doi:10.24272/j.issn.2095-8137.2021.126

Yong Cui, 华南师范大学生命科学学院昆虫科学与技术研究所，广东省昆虫发育生物学与应用技术重点实验室，广州市昆虫发育调控与应用研究重点实验室，广东广州 510631，中国 + Show 13 more

Open Access

https://doi.org/10.24272/j.issn.2095-8137.2021.126

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Abstract

The insect brain is the central part of the neurosecretory system, which controls morphology, physiology, and behavior during the insect’s lifecycle. Lepidoptera are holometabolous insects, and their brains develop during the larval period and metamorphosis into the adult form. As the only fully domesticated insect, the Lepidoptera silkworm Bombyx mori experienced changes in larval brain morphology and certain behaviors during the domestication process. Hormonal regulation in insects is a key factor in multiple processes. However, how juvenile hormone (JH) signals regulate brain development in Lepidoptera species, especially in the larval stage, remains elusive. We recently identified the JH receptor Methoprene tolerant 1 (Met1) as a putative domestication gene. How artificial selection on Met1 impacts brain and behavioral domestication is another important issue addressing Darwin’s theory on domestication. Here, CRISPR/Cas9-mediated knockout of Bombyx Met1 caused developmental retardation in the brain, unlike precocious pupation of the cuticle. At the whole transcriptome level, the ecdysteroid (20-hydroxyecdysone, 20E) signaling and downstream pathways were overactivated in the mutant cuticle but not in the brain. Pathways related to cell proliferation and specialization processes, such as extracellular matrix (ECM)-receptor interaction and tyrosine metabolism pathways, were suppressed in the brain. Molecular evolutionary analysis and in vitro assay identified an amino acid replacement located in a novel motif under positive selection in B. mori, which decreased transcriptional binding activity. The B. mori MET1 protein showed a changed structure and dynamic features, as well as a weakened co-expression gene network, compared with B. mandarina. Based on comparative transcriptomic analyses, we proposed a pathway downstream of JH signaling (i.e., tyrosine metabolism pathway) that likely contributed to silkworm larval brain development and domestication and highlighted the importance of the biogenic amine system in larval evolution during silkworm domestication.

Highlights

The insect brain is the central part of the neurosecretory system, which controls morphology, physiology, and behavior during the insect’s lifecycle
Given that the role of juvenile hormone (JH) and its receptor Methoprene tolerant 1 (Met1) in the silkworm early larval stage remains elusive (Daimon et al, 2015) and that the mosaic mutants showed a clear phenotype of precocious metamorphosis of the cuticle, we used these mutants for further analysis
Based on the above evidence showing that Met1 promotes silkworm larval brain development, and that the larval brain of domestic B. mori has fewer connections between the two lobes compared with wild B. mandarina (Figure 1), we further explored how artificial selection affected the biological function of Met1 during silkworm brain domestication