Nonrandom distribution of histone mRNAs into polysomes and nonpolysomal ribonucleoprotein particles in sea urchin embryos.

In the early sea urchin embryo, newly synthesized cytoplasmic histone mRNA is found both on polysomes and free of ribosomes as nonpolysomal messenger ribonucleoprotein particles (free RNPs). The distribution of newly synthesized histone mRNAs between translating and nontranslating compartments is nonrandom and dependent on the developmental stage. Gel electrophoresis and autoradiography of polysomal and free RNP RNA from embryos at various stages show that (i) the fraction of total newly synthesized histone mRNA that is in polysomes is greater than the fraction of total newly synthesized poly(A)+mRNA that is in polysomes, at all stages examined, and (ii) among the five histone mRNAs. H1 mRNA and H4 mRNA are relatively more enriched in the free RNPs than are the mRNAs for H2A, H2B, and H3. These data suggest that histone mRNA, as a class, is more efficiently utilized as a template than the average mRNA and, of the cytoplasmic histone mRNAs, the mRNAs for histones H2A, H2B, and possibly H3 are selected more frequently for translation than those for H1 and H4. Cell-free translations of polysomal and free RNP RNAs yield different ratios of in vitro histone products, consistent with the RNA distribution data. To test the possibility that the in vivo distribution of the histone mRNAs is the consequence of different intrinsic initiation capabilities of the individual mRNAs, ribosome-binding assays were carried out and unequal binding abilities of the histone mRNAs in the reticulocyte lysate were shown. A translational level component in the regulation of histone synthesis in the sea urchin embryo is indicated.