Kiichiro Taniguchi, Akihiko Kokuryo, Takao Imano, Ryunosuke Minami, Hideki Nakagoshi and Takashi Adachi-Yamada
Although most animal cells possess only a single nucleus, some cells such as myocytes and hepatocytes show sporadic occurrences of multiple nuclei. The Drosophila adult male accessory gland, an internal reproductive organ for production of seminal fluid components, displays an exceptional columnar epithelium where all cells have two nuclei. Despite this striking feature, no adaptive significances to account for binucleation have been proposed.
We demonstrate that one possible purpose of binucleation is enabling plasticity in organ size. To compare various cytological traits between binucleate and mononucleate states, we artificially converted the cellular state from the binucleate state to either the endoreplicated mononucleate or pseudodivided mononucleate state in the accessory gland epithelium by genetically manipulating the spindle assembly checkpoint. Depending on the flies’ age and mating and feeding conditions, the apical area of the binucleate cells enlarges compared with that of endoreplicated mononucleate cells. On the other hand, the apical area shrinks after mating compared with that of divided mononucleate cells. Consequently, this wide range of apical area size in binucleate cells increases the plasticity in organ size compared with that in endoreplicated mononucleate and divided mononucleate cells. The highly plastic features in an organ composed of binucleate cells should lead to higher rates of reproductive success in response to nutrition uptake and mating frequency. Similar plasticity might also be beneficial in hepatocytes and myocytes, both of which show great variability in cell size. Our results provide direct evidence that cell-size plasticity is a basis of multinucleation in animal cells.