Estrogen-Related Receptor Influences the Hemolymph Glucose Content by Regulating Midgut Trehalase Gene Expression in the Last Instar Larvae of Bombyx mori

Abstract

The expression of trehalase in the midgut of insects plays an important role in glucose supply to the hemolymph. Energy metabolism is usually regulated by the estrogen-related receptor (ERR). A decrease in ATP levels is caused by the ERR hindering glycolysis. However, the relationship between trehalose accumulation and ERR expression is still unclear. Here, we found that silkworm ERR (BmERR) is concentrated and BmERR expression is strongly correlated with trehalase in the midgut during the last instar silkworm larval stage. We cloned the promoter of the trehalase from Bombyx mori (BmTreh) and found that the ERR bound directly to the core response elements of the promoter. Cell level interference and the overexpression of ERR can reduce or enhance BmTreh transcription and promoter activity. Overexpressed transgenic BmERR can significantly increase the expression of BmTreh in the midgut of the last instar silkworm larvae, thereby hydrolyzing trehalose into glucose and releasing it into the hemolymph. Additionally, increased hemolymph glucose content reduces silkworm pupa weight but does not affect silk protein production from the silk gland. Our results suggest a novel function for BmERR through its involvement in BmTreh regulation and expand the understanding of ERR functions in insect trehalose metabolism.

The Response of the Estrogen-Related Receptor to 20-Hydroxyecdysone in Bombyx mori: Insight Into the Function of Estrogen-Related Receptor in Insect 20-Hydroxyecdysone Signaling Pathway

“…In addition, ERR was involved in carbohydrate metabolism, hypoxic metabolism and energy metabolism in Drosophila ( Tennessen et al, 2011 ; Li et al, 2013 ; Kovalenko et al, 2019 ). Our previous research also found that BmERR regulated the expression of glycolysis-related genes to participate in the development of silkworm embryos, and affected the glucose concentration in the midgut by regulating the expression of trehalase ( Long et al, 2020 ; Shen et al, 2021 ). These further implied that ERR might regulate 20E signaling by mediating nutritional metabolism, then affects insulin pathway and finally exerts its influence on 20E signaling.…”

“…Since the completion of the genome sequence, the silkworm ( Bombyx mori ) has become a widely used model insect for lepidopteran research, and a general model organism for life sciences, toxicology, and fungal infections ( International Silkworm Genome, 2008 ; Suetsugu et al, 2013 ; Meng et al, 2017 ; Abdelli et al, 2018 ; Nakajima et al, 2018 ; Matsumoto and Sekimizu, 2019 ). In previous research, we have demonstrated that the Bombyx mori ERR (BmERR) is involved in the growth and development of silkworm embryos and larvae by regulating the expression of glucose metabolism-related genes ( Long et al, 2020 ; Shen et al, 2021 ). and vitellogenin via the 20-hydroxyecdysone (20E) -EcR pathway in silkworm ( Shen et al, 2018 ).…”

Nilaparvata lugens ERR2 regulates moulting and ovary development is related to hormone signalling

“…DERR initiates the expression of pentose phosphate pathway (PPP)‐phosphogluconate dehydrogenase (PGD) in the fat body, a key enzyme in the PPP, which is essential for insect growth and energy storage (Beebe et al, 2020; Kovalenko et al, 2019). Bombyx mori ERR affects haemolymph glucose level (Shen et al, 2021). During the embryonic development of silkworm and Drosophila , ERR can directly regulate the expression of related genes in the glycolytic pathway, and the embryo uses glycogen provided by the mother for glycolysis (Long et al, 2020).…”

Identification of genes associated with the silk gland size using multi‐omics in silkworm (Bombyx mori)

“…In the larval stage, silk gland weight increases by increasing cell volume, becoming the heaviest organ, which will affect silk yield (Liang et al, 2018;Shen et al, 2021).…”

“…The silk gland begins to become morphologically different at approximately 8 days after egg laying through the division of apical cells (Dhawan & Gopinathan, 2003). In the larval stage, silk gland weight increases by increasing cell volume, becoming the heaviest organ, which will affect silk yield (Liang et al, 2018; Shen et al, 2021).…”