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

Abstract

DELLA proteins are land-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 non-vascular land plants, which lack active gibberellins or a proper GID1 receptor. Current knowledge indicates that DELLAs are important pieces of the signalling 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 non-vascular land plants for their function in transcriptional co-activation, which allowed subsequent exaptation for the interaction with the GID1 receptor when vascular plants developed gibberellin synthesis and the corresponding perception module.

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

“…In land plants, they have functionally diversified to regulate processes that are inherent to complex multicellular body plans and three-dimensional architecture, including meristem development, controlling cell division and expansion in roots and shoots, vascular development and seed maturation, as well as stress responses (Bolle, 2004; Ma et al, 2010). This functional divergence was hypothesized to occur after terrestrialization, as algal GRAS proteins form a monophyletic clade located outside of the land plant group (Hernandez-Garcia et al, 2019). However, we found that while most P. margaritaceum GRAS proteins clustered within the algal group (Fig.…”

“…However, while GRAS TFs are particualarly abundant in P . margaritaceum , none has the key N-terminal domain for interaction with the GID1 GA receptor (Hernández-García, et al 2019). Our data are congruent with the idea that the DELLA proteins emerged in the land plant ancestor where they evolved a transciptional regualtory function, and were then recruited to form the GID1-DELLA signaling with the emergence of vascular land plants (Hernández-García, et al 2019).…”

Molecular Cloning and Functional Characterization of the DELLA Gene Family in Liriodendron Hybrids

“…The second clade contained DELLAs from plants belonging to monocotyledons. Interestingly, LhSLRL together with Physcomitrella patens DELLAa, P. patens DELLAb, Selaginella kraussiana DELLA, Amborella trichopoda RHT1, Aquilegia coerulea DELLA3, Nelumbo nucifera GAI-like, and N. nucifera SLR1-like formed a clade, here named outgroup [19]. In the sequence alignment analysis, the DELLA motifs in LhSLRL in outgroup differed from those in the first clade ( Figure 2).…”

Looking back to look forward: protein–protein interactions and the evolution of development

“…While DELLA genes are ancient, the interaction between DELLA and GID1 probably emerged only after the divergence of mosses (Hirano et al ., ; Yasumura et al ., ; Cox, ; Hernandez‐Garcia & Briones‐Moreno, ). Intriguingly, DELLA domains from the hornwort Nothoceros vincentianus , the moss Physcomitrella patens , the lycophyte Selaginella moellendorffii and from A. thaliana can all act as transcriptional activation domains (Fig.…”

“…). This suggests DELLA's role in GA signaling was exapted from an ancient role as a transcriptional activator (Hernandez‐Garcia & Briones‐Moreno, ). Indeed, della mutants in P. patens do not exhibit increased growth, but P. patens DELLA proteins can trigger growth repression in A. thaliana (Yasumura et al ., ).…”