The relationship between cell proliferation and the amount and diversity of polyribosome-associated poly(A)-containing mRNA [poly(A)+ mRNA] was investigated using a cloned adenylate kinase resistant (AKR)-mouse embryo cell culture system. An early response to the stimulation of proliferation of AKR-2B cells in culture is a rapid increase in the rate of accumulation of polyribosomal poly(A)+ mRNA. This results in a large increase in the total poly(A)+ mRNA content of rapidly proliferating cells compared to that found in resting cells. The total amount of unique DNA sequence contributing to the poly(A)+ mRNA populations of both growing and resting cells is not detectably different. This corresponds to 9000-11,000 diverse gene equivalents of DNA and represents the transcription of 0.8-0.9% of the haploid mouse genome. Most of the increased poly(A)+ mRNA content of growing cells ( > 90%) reflects an increased rate of production of polysomal mRNA species which are also found in resting cells. Growing cells appear to contain some species of poly(A)+ mRNA which are either absent or present in very low concentrations in non-growing cells. Within the limits of detection, all species of poly(A)+ mRNA present in non-growing cells are also present in growing cells.