Origin and evolution of gibberellin signaling and metabolism in plants

Gibberellins modulate multiple aspects of plant behavior. The molecular mechanism by which these hormones are perceived and how this information is translated into transcriptional changes has been elucidated in vascular plants: gibberellins are perceived by the nuclear receptor GID1, which then interacts with the DELLA nuclear proteins and promote their degradation, resulting in the modification of the activity of transcription factors with which DELLAs interact physically. However, several important questions are still pending: how does a single molecule perform such a vast array of functions along plant development? What property do gibberellins add to plant behavior? A closer look at gibberellin action from an evolutionary perspective can help answer these questions. DELLA proteins are conserved in all land plants, and predate the emergence of a full gibberellin metabolic pathway and the GID1 receptor in the ancestor of vascular plants. The origin of gibberellin signaling is linked to the exaptation by GID1 of the N-terminal domain in DELLA, which already acted as a transcriptional coactivator domain in the ancestral DELLA proteins. At least the ability to control plant growth seems to be encoded already in the ancestral DELLA protein too, suggesting that gibberellins’ functional diversity is the direct consequence of DELLA protein activity. Finally, comparative network analysis suggests that gibberellin signaling increases the coordination of transcriptional responses, providing a theoretical framework for the role of gibberellins in plant adaptation at the evolutionary scale, which further needs experimental testing.