Control of development of the oral apparatus of Paramecium during sexual reproduction: An embryological perspective

Abstract

This study shows that development of the new soma during sexual reproduction in ciliates can be conceptualized on the same basis as embryogenesis in multicellular organisms. In conjugating Paramecium, development of a new oral apparatus takes place during fertilization and the first three divisions of the zygotic nucleus and completes well before the postsexual cell undergoes the first cell fission. The control of oral development is analyzed by microsurgical removal of the zygotic nucleus or the postzygotic nuclei from conjugants. The enucleated exconjugants can pass through an early hurdle in oral development (the initiation of oral membranelle assembly) and subsequently develop an oral apparatus. Such oral apparatuses nevertheless exhibit structural and functional abnormalities including fragmentation and misalignment of oral membranelles, absence of the postoral microtubular bundle, reduction in the length of buccal cavity, and impaired phagocytosis. Other stomatogenic aspects, such as the arrangement of basal bodies in the oral membranelles, remain unaffected. The two groups of exconjugants, one derived from cells enucleated at the zygotic stage, and the other at the postzygotic stage, exhibit the same types of oral abnormality. We conclude that (i) the zygotic nucleus is not essential for the initiation of oral membranelle assembly. The existence of zygotic signals for subsequent oral development is not ruled out, but these are insufficient. (ii) Postzygotic nuclei, as well as maternal nuclei (the old somatic nucleus and meiotic derivatives of the germ nucleus), control oral development. This reveals a parallelism between postsexual development in ciliates and the early embryology of multicellular organisms, in their reliance on information provided by maternal, as well as early postzygotic nuclei. (iii) The activity of the old somatic nucleus alone is not sufficient for the later stages of oral development. Probably, some stomatogenic functions of the old somatic nucleus normally utilized for the later stages of oral development in binary fission are inactivated during sexual reproduction. Alternatively, the old somatic nucleus may rely on some critical conditions prescribed by the postzygotic nuclei in order to act.