Step-by-Step Acquisition of the Gibberellin-DELLA Growth-Regulatory Mechanism during Land-Plant Evolution

Abstract

Angiosperms (flowering plants) evolved relatively recently and are substantially diverged from early land plants (bryophytes, lycophytes, and others [1]). The phytohormone gibberellin (GA) adaptively regulates angiosperm growth via the GA-DELLA signaling mechanism [2-7]. GA binds to GA receptors (GID1s), thus stimulating interactions between GID1s and the growth-repressing DELLAs [8-12]. Subsequent 26S proteasome-mediated destruction of the DELLAs promotes growth [13-17]. Here we outline the evolution of the GA-DELLA mechanism. We show that the interaction between GID1 and DELLA components from Selaginella kraussiana (a lycophyte) is GA stimulated. In contrast, GID1-like (GLP1) and DELLA components from Physcomitrella patens (a bryophyte) do not interact, suggesting that GA-stimulated GID1-DELLA interactions arose in the land-plant lineage after the bryophyte divergence ( approximately 430 million years ago [1]). We further show that a DELLA-deficient P. patens mutant strain lacks the derepressed growth characteristic of DELLA-deficient angiosperms, and that both S. kraussiana and P. patens lack detectable growth responses to GA. These observations indicate that early land-plant DELLAs do not repress growth in situ. However, S. kraussiana and P. patens DELLAs function as growth-repressors when expressed in the angiosperm Arabidopsis thaliana. We conclude that the GA-DELLA growth-regulatory mechanism arose during land-plant evolution and via independent stepwise recruitment of GA-stimulated GID1-DELLA interaction and DELLA growth-repression functions.

The Gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution

“…7): The common ancestor of basal land plants before the separation of the mosses had GAMYB-mediated regulation in the proto-tapetal cells (spore sac cells) and spores for spore outer wall formation. At this stage, the GAMYB-mediated regulation of spore outer wall formation was independent of the GA signalling pathway, as the GA signalling pathway had not yet been established 13,14 . Consistent with this hypothesis, it is reported that the disruption of multiple DELLA-like genes in P. patens did not affect the plant's life cycle 14 , and that the disruption of PpCPS/KS, which encodes ent-kaurene synthase, an enzyme essential for GA synthesis in flowering plants, did not result in abnormal spore development 36 .…”

“…At this stage, the GAMYB-mediated regulation of spore outer wall formation was independent of the GA signalling pathway, as the GA signalling pathway had not yet been established 13,14 . Consistent with this hypothesis, it is reported that the disruption of multiple DELLA-like genes in P. patens did not affect the plant's life cycle 14 , and that the disruption of PpCPS/KS, which encodes ent-kaurene synthase, an enzyme essential for GA synthesis in flowering plants, did not result in abnormal spore development 36 . In the next step, the common ancestor of basal vascular plants before the separation of the lycopsids acquired GA biosynthesis and GA signalling pathways to regulate the pre-existing GAMYB-mediated system, leading to the establishment of the GA signalling pathway via GAMYB.…”

“…During the divergence of basal vascular plants including lycopods from the moss lineage, a GA receptor, GID1 and DELLA repressors were established as key components for GA perception system in association with a functional GA biosynthetic pathway, indicating the occurrence of the entire GA signalling pathway 13,14 . However, the biological function of GA in basal vascular plants has been unclear, as GA treatment does not cause any developmental defects at the vegetative stage, such as increased stem or leaf elongation, in Selaginella 13 .…”

“…We first examined the expression pattern of PpGAMYBs to estimate the biological function of PpGAMYBs in P. patens, which has no functional GA perception system and GA biosynthetic pathway 13,14 (Fig. 4a,b).…”

“…Previous anatomical and in silico studies suggest that, similar to flowering plants, present-day bryophytes, including mosses, and lycophytes (lycopods) contain sporopollenin-containing outer walls on the surface of their spores and microspores [9][10][11] , and genes encoding CYP703 homologues have been detected in these genomes 12 . Curiously, however, one of the basal vascular plants, Selaginella, contains a functional GA perception system that is mediated by a GA receptor, GIBBERELLIN-INSENSITIVE DWARF1 (GID1), and suppressor proteins (DELLAs), whereas one of the basal land plants, Physcomitrella patens, does not contain this system [13][14][15][16] . These observations led us to speculate that the ancestral land plants developed sporopollenin-containing outer walls on their spores, which protected the spores from dryness and ultraviolet radiation on land, in association with CYP703-like enzymes, and that GA signalling pathway then evolved to control the development of the spore outer wall via the modulation of CYP703-like expressions during the evolution from mosses to lycopods.…”