Glycogen and Glucose Metabolism Are Essential for Early Embryonic Development of the Red Flour Beetle Tribolium castaneum

Abstract

Control of energy metabolism is an essential process for life. In insects, egg formation (oogenesis) and embryogenesis is dependent on stored molecules deposited by the mother or transcribed later by the zygote. In oviparous insects the egg becomes an isolated system after egg laying with all energy conversion taking place during embryogenesis. Previous studies in a few vector species showed a strong correlation of key morphogenetic events and changes in glucose metabolism. Here, we investigate glycogen and glucose metabolism in the red flour beetle Tribolium castaneum, an insect amenable to functional genomic studies. To examine the role of the key enzymes on glycogen and glucose regulation we cloned and analyzed the function of glycogen synthase kinase 3 (GSK-3) and hexokinase (HexA) genes during T. castaneum embryogenesis. Expression analysis via in situ hybridization shows that both genes are expressed only in the embryonic tissue, suggesting that embryonic and extra-embryonic cells display different metabolic activities. dsRNA adult female injection (parental RNAi) of both genes lead a reduction in egg laying and to embryonic lethality. Morphological analysis via DAPI stainings indicates that early development is impaired in Tc-GSK-3 and Tc-HexA1 RNAi embryos. Importantly, glycogen levels are upregulated after Tc-GSK-3 RNAi and glucose levels are upregulated after Tc-HexA1 RNAi, indicating that both genes control metabolism during embryogenesis and oogenesis, respectively. Altogether our results show that T. castaneum embryogenesis depends on the proper control of glucose and glycogen.

Inorganic Polyphosphates Regulate Hexokinase Activity and Reactive Oxygen Species Generation in Mitochondria of Rhipicephalus (Boophilus) microplus Embryo

“…Tick embryogenesis is characterized by the formation of a cellularized blastodermal cell layer up to day 4. Thereafter, the embryo starts segment formation and initiates organogenesis 24, 54. Previously, we provided evidence that mitochondrial membrane PPX plays a role in energy metabolism in R. microplus during embryo development 18.…”

“…2.7.1.1; HK). This enzyme has been characterized in several organisms 19-24. Four distinct hexokinase isozymes are reported for mammalian tissues and are named types I-IV.…”

Rhodnius prolixus: From classical physiology to modern developmental biology

“…Recent years have witnessed a steadily growing interest in the interplay between embryonic development and metabolism. For instance, recent reports show that glucose metabolism is essential for early embryonic development in Tribolium (Fraga et al ., ) and that GSK3 controls mitochondrial function and glucose metabolism during oocyte maturation in Drosophila (Sieber et al ., ). In Rhodnius , in view of the potential for biological control of Chagas disease spread, the metabolic pathways linking blood ingestion and the development of eggs and embryos have been widely investigated (references in (Atella et al ., ).…”

Glycogen content relative to expression of glycogen phosphorylase (GPH) and hexokinase (HK) during the reproductive cycle in the Fujian Oyster, Crassostrea angulata

“…A simplified model of energy utilization and glycogen mobilization in the glycolytic pathway showed that glycogen storage is mobilized into the glycolytic pathway through the actions of glycogen phosphorylase (GPH) and hexokinase (HK) (Fraga et al, 2013). Its synthesis is regulated by glycogen synthase (GYS) (Bacca et al, 2005).…”

“…Glycogen breakdown generates glucose, which enters the glycolytic pathway and is converted to pyruvate (Fraga et al, 2013). This process leads to the generation of ATP.…”