The induction of ribosome biosynthesis in a nonmitotic secretory tissue

Many investigations of the biosynthesis of ribosomes have revealed that ribosome numbers increase with growth rate in a parallel fashion. However, we have now shown that there is also a need for active ribosome synthesis in a nonmitotic tissue which is induced to secrete. The paragonial glands of Drosophila melanogaster produce and secrete proteins that are found in the seminal fluid. Following even a single copulation event these glands are substantially reduced in size, but rapidly refill, synthesizing new secretion proteins (Chen, P.S. 1980) in Invertebrate Systems in Vitro (Kurstak, E., Maramorosch, K., and Dubendorfer, A., eds) pp. 303-313, Elsevier, Amsterdam) Anticipating that paragonial gland cells might require more ribosomes to accomplish this burst of protein synthesis, we injected 10-day-old adult male flies with either [32P] phosphate or [35S]methionine, allowed them to copulate (40 +/- 20 min after injection), and then measured the amounts of rRNA and ribosomal protein synthesis taking place with time. There is clearly a burst of ribosome synthesis starting as early as 30 min after copulation and declining after 6 h. This is evidenced by the coordinate accumulation of labeled rRNAs and ribosomal proteins. However, further experiments showed that there is no concomitant rise in the accumulation of ribosomal protein mRNAs. This suggests that these mRNAs are underutilized in the paragonial glands before copulation and more actively translated after copulation. A stimulation of translation of ribosomal proteins is then well-coordinated with increased rRNA transcription, but an increase of ribosomal protein mRNAs is not coordinated with these events. Both the up- and down-regulation of ribosome biosynthesis need not be coupled to cell growth or a specific developmental schedule, but rather may be due to the need for secretory protein synthesis.