The mouse egg contains about 90,000 mitochondria which undergo a buildup of mitochondrial cristae and increase in respiratory activity during cleavage. The mitochondrial DNA does not replicate during preimplantation development but is transcribed actively from the two-cell stage onward (Pikó and Taylor, 1987: Dev Biol 123:364-374). To gain further insight into mitochondrial biogenesis, we have now determined the steady state amounts of the mRNAs for the cytochrome c oxidase (COX) subunits IV, Vb and VIIc and the H(+)-ATPase subunit 9 (P1) (all encoded by nuclear genes) in slot hybridization experiments of total RNA from oocytes and early embryos. All four mRNAs showed a similar developmental pattern of prevalence, characterized by a steady decline in mRNA copy numbers from the late growth-phase oocyte through the two-cell embryo, and an about 30-fold rise during cleavage through the blastocyst stage. However, the ATPase subunit 9 (P1) mRNA was about three times more prevalent in cleavage-stage embryos than the COX mRNAs. A similar pattern was obtained previously for the mitochondrial-encoded COX I and II mRNAs, but the latter accumulate at a 30-50-fold excess over the nuclear-encoded COX subunit mRNAs during the cleavage stages. The results suggest a coordinated activation and transcription of the mitochondrial and nuclear genes for the components of the respiratory apparatus beginning with the two-cell stage. It is estimated that new respiratory chains are produced at a rate of 50-100 chains hr-1/mitochondrion in the early blastocyst, accounting for 3.5-7% of the total protein synthetic activity at this stage.(ABSTRACT TRUNCATED AT 250 WORDS)