Comparative Proteomic Analysis Provides New Insights into the Molecular Basis of Thermal-Induced Parthenogenesis in Silkworm (Bombyx mori)

SIMPLE SUMMARY: Parthenogenesis is a reproductive mode by which an oocyte goes into development without fertilization, which is common in insects and plays an important role in evolution, sociality, and ecology. However, the molecular mechanism of parthenogenesis in insects remains to be expanded. The silkworm Bombyx mori is an economically important insect. The artificial parthenogenesis induced in vitro using thermal stimuli has been well used in silkworm breeding as a sex control method. A better understanding of parthenogenesis and its regulatory mechanisms could benefit sericultural production. Meanwhile, silkworm provides a good material for parthenogenesis development research as a lepidopteran model. In this study, iTRAQ-based quantitative proteomics were carried out to compare the protein expression profile between a fully parthenogenetic line (PL) and its parent amphigenetic line (AL). We identified 274 increased abundance proteins and 211 decreased abundance proteins before thermal induction, and 97 increased abundance proteins and 187 decreased abundance proteins after thermal induction in PL. Function analysis uncovered the molecular signatures underlying the two different reproductive modes, and the proteins and pathways involved in a meiosis process response to thermal stimuli. The results provide new insights into the molecular mechanism underlying silkworm parthenogenesis. ABSTRACT: Artificial parthenogenetic induction via thermal stimuli in silkworm is an important technique that has been used in sericultural production. However, the molecular mechanism underlying it remains largely unknown. We have created a fully parthenogenetic line (PL) with more than 85% occurrence and 80% hatching rate via hot water treatment and genetic selection, while the parent amphigenetic line (AL) has less than 30% pigmentation rate and less than 1% hatching rate when undergoing the same treatment. Here, isobaric tags for relative and absolute quantitation (iTRAQ)-based analysis were used to investigate the key proteins and pathways associated with silkworm parthenogenesis. We uncovered the unique proteomic features of unfertilized eggs in PL. In total, 274 increased abundance proteins and 211 decreased abundance proteins were identified relative to AL before thermal induction. Function analysis displayed an increased level of translation and metabolism in PL. After thermal induction, 97 increased abundance proteins and 187 decreased abundance proteins were identified. An increase in stress response-related proteins and decrease in energy metabolism suggested that PL has a more effective response to buffer the thermal stress than AL. Cell cycle-related proteins, including histones, and spindle-related proteins were decreased in PL, indicating an important role of this decrease in the process of ameiotic parthenogenesis.