BACKGROUND Mammals have two types of full-grown oocytes: those with germinal vesicles (GVs) in which the chromatin is condensed and surrounds the nucleolus (surrounded-nucleolus (SN)-type) and those in which the chromatin is less condensed and does not surround the nucleolus (non-surrounded-nucleolus (NSN)-type). Although SN oocytes possess higher meiotic and developmental competence than NSN oocytes, the factors underlying this difference are unknown. METHODS AND RESULTS The GVs of murine SN and NSN oocytes were exchanged by nuclear transfer and the nucleus/cytoplasm of each reconstructed oocyte was classified as follows: SN/SN, NSN/SN, SN/NSN or NSN/NSN. After reconstruction, the meiotic maturation and preimplantation development of the oocytes were analysed. Few mature SN/NSN and NSN/NSN oocytes were observed (20–26%). In contrast, 88% of the NSN/SN oocytes matured; however, they rarely developed to the blastocyst stage after fertilization (4%), whereas most of the SN/SN oocytes matured (84%) and reached the blastocyst stage (83%). When the metaphase II (MII) plates of in vitro-matured NSN/SN oocytes were transferred into enucleated MII oocytes in which the contents of the SN-type GVs were spread into the cytoplasm, they completed full-term development. CONCLUSIONS The differences in meiotic and developmental competence between SN and NSN oocytes are determined by factors in the cytoplasm and nucleus, respectively. In addition, material(s) within SN-type GVs, and not the chromatin configuration itself, is essential for full-term development.