Steroid hormone ecdysone deficiency stimulates preparation for photoperiodic reproductive diapause

Abstract

Diapause, a programmed developmental arrest primarily induced by seasonal environmental changes, is very common in the animal kingdom, and found in vertebrates and invertebrates alike. Diapause provides an adaptive advantage to animals, as it increases the odds of surviving adverse conditions. In insects, individuals perceive photoperiodic cues and modify endocrine signaling to direct reproductive diapause traits, such as ovary arrest and increased fat accumulation. However, it remains unclear as to which endocrine factors are involved in this process and how they regulate the onset of reproductive diapause. Here, we found that the long day-mediated drop in the concentration of the steroid hormone ecdysone is essential for the preparation of photoperiodic reproductive diapause in Colaphellus bowringi, an economically important cabbage beetle. The diapause-inducing long-day condition reduced the expression of ecdysone biosynthetic genes, explaining the drop in the titer of 20-hydroxyecdysone (20E, the active form of ecdysone) in female adults. Application of exogenous 20E induced vitellogenesis and ovarian development but reduced fat accumulation in the diapause-destined females. Knocking down the ecdysone receptor (EcR) in females destined for reproduction blocked reproductive development and induced diapause traits. RNA-seq and hormone measurements indicated that 20E stimulates the production of juvenile hormone (JH), a key endocrine factor in reproductive diapause. To verify this, we depleted three ecdysone biosynthetic enzymes via RNAi, which confirmed that 20E is critical for JH biosynthesis and reproductive diapause. Importantly, impairing Met function, a component of the JH intracellular receptor, partially blocked the 20E-regulated reproductive diapause preparation, indicating that 20E regulates reproductive diapause in both JH-dependent and -independent manners. Finally, we found that 20E deficiency decreased ecdysis-triggering hormone signaling and reduced JH production, thereby inducing diapause. Together, these results suggest that 20E signaling is a pivotal regulator that coordinates reproductive plasticity in response to environmental inputs.

Neuroendocrine Regulation of Reproductive Dormancy in the Fruit Fly Drosophila melanogaster: A Review of Juvenile Hormone-Dependent Regulation

“…Interestingly, a recent study has shown that ecdysteroids regulate dormancy via ETH in the cabbage beetle Colaphellus bowringi (Guo et al, 2021). In this insect, reduction of ecdysteroid biosynthesis is required for suppressed oogenesis and accumulated lipid storage in the fat body in dormancyinducing conditions.…”

Topical Application of Synthetic Hormones Terminated Reproductive Diapause of a Univoltine Weed Biological Control Agent

“…Thus, application of methoprene alone is expected to produce only a temporary effect. However, 20E is thought to block activation of JH esterase, and it may also stimulate production of JH [ 23 , 31 ]. This is consistent with the result that the number of feeding holes and oviposition were higher for the 2M (20E + methoprene) treatment than the AM (methoprene) treatment in Experiment 3.…”

“…Reproductive diapause of insects is generally regulated by two hormones: juvenile hormone (JH) secreted from the corpora allata (CA) and ecdysone secreted from both the prothoracic gland in larval stages [ 7 , 22 ] and reproductive organs including the ovaries of females and accessary glands of males [ 23 , 24 ]. Reduced JH titer induces reproductive diapause [ 25 , 26 ], which is caused by either JH esterase activity [ 27 , 28 ] or blocking the JH biosynthesis pathway [ 29 ].…”

“…Reduced JH titer induces reproductive diapause [ 25 , 26 ], which is caused by either JH esterase activity [ 27 , 28 ] or blocking the JH biosynthesis pathway [ 29 ]. Further, 20-hydroxyecdysone (20E), which is the active form of ecdysone, is necessary for JH production and terminating reproductive diapause [ 23 ]. Methoprene, which is the closest structurally to natural JH among synthetic JH analogs, has been used as an insecticide in the insect growth regulator class [ 30 ].…”

Role of Endocrine System in the Regulation of Female Insect Reproduction

“…However, 20E might also repress lipid accumulation and could be independent of JH signaling. Therefore, it was suggested that the 20E controls the photoperiodic reproductive diapause of C. bowringi in both JH-dependent and JH-independent manners [38]. ETH plays a crucial role in the maintenance of juvenile hormone acid methyltransferase (JHAMT), which in turn is required for the normal production of JHs, vitellogenesis, and reproduction [39].…”