Evolution and diversification of the plant gibberellin receptor GID1

Yoshida, Hideki; Tanimoto, Eiichi; Hirai, Takanori; Miyanoiri, Yohei; Mitani, Rie; Kawamura, Morio; Takeda, Mitsuhiro; Takehara, Shoichiro; Hirano, Ken; Kainosho, Masatsune; Akagi, Takashi; Matsuoka, Makoto; Ueguchi-Tanaka, Miyako

doi:10.1073/pnas.1806040115

Cited by 60 publications

(58 citation statements)

References 38 publications

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“…Therefore, at least two possible models can be contemplated: either GA signaling emerged in a common ancestor of hornworts and vascular plants, or it emerged independently in vascular plants and in hornworts, and the similar behaviour is caused by functional convergence. A third possibility would be that a putative GAindependent GID1-DELLA module in the ancestor of all land plants would have been lost in different clades, but this is highly unlikely based on recent evidence about GID1 evolution (Yoshida et al 2018). The origin of the participation of DELLAs in GA signaling requires a more complete picture.…”

Section: Discussionmentioning

confidence: 99%

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

Hernández-García

Briones‐Moreno

Dumas

et al. 2019

Molecular Biology and Evolution

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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.

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Section: Discussionmentioning

confidence: 99%

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

Hernández-García

Briones‐Moreno

Dumas

et al. 2019

Molecular Biology and Evolution

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“…Though the gibberellin precursor pool (GA9, GA19 and GA20) appeared higher in the evening, no significant differences were observed between timepoints nor between light levels ( Figure 4A). The bioactive gibberellins differ in their affinity for the receptor GID1, with GA3 and GA1 having a weak affinity compared to strong binding affinity of GA4 (16)(17). The low affinity bioactive gibberellins (GA1 and GA3) had no clear differences between treatments (Supplemental Figure 4).…”

Section: Bioactive Gibberellins Accumulate During the Night And Are Smentioning

confidence: 98%

“…The final step to bioactive gibberellin is catalysed by GIBBERELLIN 3-BETA-DIOXYGENASE (GA3ox) (11). In higher plants GA4, GA1 and GA3 have been confirmed to bind the GIBBERELLIN INSENSTIVE DWARF1 (GID1) receptor (16)(17). These bioactive gibberellins can also be made inactive by the enzyme GA2ox (11).…”

Section: Introductionmentioning

confidence: 99%

Nighttime gibberellin biosynthesis is influenced by fluctuating environmental conditions and contributes to growth adjustments of Arabidopsis leaves

Prasetyaningrum

Mariotti

et al. 2020

Preprint

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Optimal plant growth performance requires that the action of growth signals, such as gibberellins (GA), are coordinated with the availability of photo-assimilates. Here, we studied the links between gibberellin biosynthesis and carbon availability, and the subsequent effects on growth. The results presented here show that carbon availability, light and dark cues, and the clock ensure the timing and magnitude of gibberellin biosynthesis and that disruption of these mechanisms results in reduced gibberellin levels and expression of downstream genes. Carbon dependent nighttime induction of GIBBERELLIN 3-BETA-DIOXYGENASE 1 (GA3ox1) was severely hampered when preceded by a day of lowered light availability, leading specifically to reduced bioactive GA4 levels, and coinciding with a decline in leaf expansion rate during the night. We attribute this decline in leaf expansion mostly to reduced photo-assimilates. However, plants where gibberellin limitation was alleviated had significantly improved expansion demonstrating the relevance of gibberellins in growth control under varying carbon availability. Carbon dependent expression of upstream gibberellin biosynthesis genes (KAURENE SYNTHASE, KS and GIBBERELLIN 20 OXIDASE 1, GA20ox1) was not translated into metabolite changes within this short timeframe. We propose a model where the extent of nighttime biosynthesis of bioactive GA4 by GA3ox1 is determined by starch, as the nighttime carbon source, and so provides day-to-day adjustment of gibberellin responses.

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“…FBP only recruits DELLA for degradation in the GA signalling pathway. To allow GA signalling through the proteolytic pathway, GA was first perceived by the GA receptor known as Gibberellin insensitive dwarf 1 (GID1), which was first found in rice (Ueguchi-Tanaka et al 2005;Shimada et al 2008;Yoshida et al 2018). In Arabidopsis, there are three GA receptors: GID1a, GID1b and GID1c (Nakajima et al 2006).…”

Section: Gibberellin Signallingmentioning

confidence: 99%

Diverse and dynamic roles of F-box proteins in plant biology

Hamid

Ahmad-Fauzi

Zainal

et al. 2020

Planta

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The SCF complex is a widely studied multi-subunit ring E3 ubiquitin ligase that tags targeted proteins with ubiquitin for protein degradation by the ubiquitin 26S-proteasome system (UPS). The UPS is an important system that generally keeps cellular events tightly regulated by purging misfolded or damaged proteins and selectively degrading important regulatory proteins. The specificity of this post-translational regulation is controlled by F-box proteins (FBPs) via selective recognition of a protein-protein interaction motif at the C-terminal domain. Hence, FBPs are pivotal proteins in determining the plant response in multiple scenarios. It is not surprising that the FBP family is one of the largest protein families in the plant kingdom. In this review, the roles of FBPs, specifically in plants, are compiled to provide insights into their involvement in secondary metabolites, plant stresses, phytohormone signalling, plant developmental processes and miRNA biogenesis. Keywords Ubiquitin 26S-proteasome system (UPS) • SCF complex • F-box protein (FBP) • Plant stresses • Phytohormone signalling • Secondary metabolites • Plant development • miRNA

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Evolution and diversification of the plant gibberellin receptor GID1

Cited by 60 publications

References 38 publications

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

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

Nighttime gibberellin biosynthesis is influenced by fluctuating environmental conditions and contributes to growth adjustments of Arabidopsis leaves

Diverse and dynamic roles of F-box proteins in plant biology

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