Glycogen and glucose metabolism are essential for early embryonic development of the red flour beetle Tribolium castaneum

PLoS One. 2013 Jun 4;8(6):e65125. doi: 10.1371/journal.pone.0065125. Print 2013.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Embryonic Development*
  • Female
  • Gene Expression Regulation, Developmental
  • Genomics
  • Glucose / metabolism*
  • Glycogen / metabolism*
  • Glycogen Synthase Kinase 3 / deficiency
  • Glycogen Synthase Kinase 3 / genetics
  • Glycogen Synthase Kinase 3 / metabolism
  • Hexokinase / deficiency
  • Hexokinase / genetics
  • Hexokinase / metabolism
  • Mothers
  • Oogenesis / genetics
  • RNA Interference
  • Tribolium / embryology*
  • Tribolium / enzymology
  • Tribolium / genetics
  • Tribolium / metabolism*

Substances

  • Glycogen
  • Hexokinase
  • Glycogen Synthase Kinase 3
  • Glucose

Grants and funding

Brazil is funded by FAPERJ, (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (Portuguese: Research Support Foundation of the State of Rio de Janeiro; Brazil)) CNPq (Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (Brazil)) and INCT-Entomologia Molecular. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.