Formation of a whorl-like autophagosome by Golgi apparatus engulfing a ribosome-containing vacuole in corpora allata of the cockroach Diploptera punctata.

Abstract

Previously, we showed that synchronous autophagy occurred in the corpora allata during the declining phase of juvenile hormone synthesis in mated adult females of the cockroach Diploptera punctata. At the onset of this process, conspicuous whorl-like autophagosomes were often observed. Each consisted of a ribosome-containing vacuole at the center surrounded by about eight layers of double membranes. Labeling the cis-Golgi cisternae with hot osmium and histochemical detection of thiamine pyrophosphatase in the trans-Golgi cisternae were used to trace the autophagic process. We conclude that the membranes surrounding the whorl-like autophagosome are derived from the entire Golgi apparatus with its cis-cisternae forming the outermost layer and the trans-cisternae the innermost layer. The engulfing process is initiated through direct contact between trans-cisternae of the Golgi apparatus and the isolation membrane of the ribosome-containing vacuole. Formation of a whorl-like autophagosome appears to be a highly regulated process specific to ribosome-containing vacuoles since it occurs only on day 5 and the Golgi apparatus does not recognize membranes of other types of autophagic vesicles or of functional organelles. This novel behavior of the Golgi apparatus in the corpora allata should play an important role in the long-term inhibition of juvenile hormone synthesis (e.g., during gestation) since it results in the depletion of cellular machinery for juvenile hormone synthesis.