Origin of Gibberellin-Dependent Transcriptional Regulation by Molecular Exploitation of a Transactivation Domain in DELLA Proteins

DELLA proteins are plant-specific transcriptional regulators known to interact through their C-terminal GRAS domain with over 150 transcription factors in Arabidopsis thaliana. Besides, DELLAs from vascular plants can interact through the N-terminal domain with the gibberellin receptor encoded by GID1, through which gibberellins promote DELLA degradation. However, this regulation is absent in nonvascular land plants, which lack active gibberellins or a proper GID1 receptor. Current knowledge indicates that DELLAs are important pieces of the signaling machinery of vascular plants, especially angiosperms, but nothing is known about DELLA function during early land plant evolution or if they exist at all in charophytan algae. We have now elucidated the evolutionary origin of DELLA proteins, showing that algal GRAS proteins are monophyletic and evolved independently from those of land plants, which explains why there are no DELLAs outside land plants. DELLA genes have been maintained throughout land plant evolution with only two major duplication events kept among plants. Furthermore, we show that the features needed for DELLA interaction with the receptor were already present in the ancestor of all land plants and propose that these DELLA N-terminal motifs have been tightly conserved in nonvascular land plants for their function in transcriptional coactivation, which allowed subsequent exaptation for the interaction with the GID1 receptor when vascular plants developed gibberellin synthesis and the corresponding perception module.