A positive feedback loop between germ cells and gonads induces and maintains cnidarian sexual reproduction

Abstract

The fertile gonad includes cells of two distinct developmental origins: the somatic mesoderm and the germline. How somatic and germ cells interact to develop and maintain fertility is not well understood. Here, using grafting experiments and transgenic reporter animals, we find that a specific part of the gonad-the germinal zone-acts as a sexual organizer to induce and maintain de novo germ cells and somatic gonads in non-sexual tissue in the cnidarian Hydractinia symbiolongicarpus. We further show that germ cells express a novel member of the TGF-{beta} family (Gonadless, Gls) that induces somatic gonad morphogenesis. Loss of Gls resulted in animals lacking somatic gonadal structures but having few, non-proliferative germ cells. We propose a model according to which a small number of primary germ cells drive gonad development though Gls morphogen secretion. The germinal zone in the newly formed gonad, in turn, provides positive feedback to induce secondary germ cells by activating Tfap2 (the master regulator of germ cell fate) in resident pluripotent stem cells. De novo induction of germ cells by gonads in adult life is absent in bilaterians with a sequestered germline. However, the contribution of germ cell signaling to the patterning of somatic gonadal tissue, as observed in Hydractinia, may be a general animal feature.