A GRAS transcription factor regulates far-red light responses via gibberellin-related compounds in Marchantia...

Gibberellin (GA)-dependent regulation of growth and development is a critical innovation for environmental adaptation that arose during the evolution of land plants. While bioactive GA molecules known in angiosperms have not been detected in bryophytes, intermediates in GA biosynthesis, such as ent-kaurenoic acid (KA), are required for bryophyte development. However, the absence of orthologs of the known GA receptor GIBBERELLIN INSENSITIVE DWARF1 (GID1) in bryophytes suggests the existence of an alternative pathway for the action of GA-related compounds. In the liverwort Marchantia polymorpha, far-red light (FR) responses are mediated by a yet-unknown GA-related compound (termed GAMp). Here we show that MpGRAS10, a GRAS family transcription factor, is likely involved in GAMp signaling. Functional analysis revealed that MpGRAS10 is required for FR responses, including hyponastic thallus growth and gametangiophore formation. The insensitivity of Mpgras10 mutants to KA suggests that MpGRAS10 acts downstream of KA biosynthesis. Moreover, MpGRAS10 gain of function caused morphological and transcriptomic changes similar to FR responses under white-light conditions, as well as increased sensitivity to KA treatment. Phylogenetic analysis demonstrated that MpGRAS10 belongs to a GRAS clade containing orthologs in bryophytes, lycophytes and ferns, but not seed plants. These findings provide insights into the diversity and evolution of GA-related signaling pathways in land plants.