Abstract Germline fate determination is a critical event in sexual reproduction. Unlike animals, plants specify the germline by reprogramming somatic cells at late stages of their development. However, the genetic basis of germline fate determination and how it has evolved during land plant evolution are still poorly understood. Here, we report that the plant homeodomain (PHD)-finger protein GERMLINE IDENTITY DETERMINANT (GLID) is a key regulator of germline specification in the liverwort Marchantia polymorpha. Loss of MpGLID function causes failure of germline initiation, leading to absence of sperm and egg cells. Remarkably, overexpression of MpGLID in M. polymorpha induces the ectopic formation of cells with male germline cell features exclusively in male thalli. We further show that MpBONOBO (BNB), with an evolutionarily conserved function, can induce the formation of male germ cell-like cells through activation of MpGLID by directly binding to its promoter. The Arabidopsis (Arabidopsis thaliana) MpGLID orthologue, MALE STERILITY1 (AtMS1), fails to replace the germline specification function of MpGLID in M. polymorpha, demonstrating that a derived function of MpGLID orthologues has been restricted to tapetum development in flowering plants. Collectively, our findings suggest the presence of the BNB-GLID module in complex ancestral land plants that has been retained in bryophytes but rewired in flowering plants for male germline fate determination.

The BNB–GLID module regulates germline fate determination in Marchantia polymorpha