Genetic Analysis Reveals That C19-GA 2-Oxidation Is a Major Gibberellin Inactivation Pathway in<i>Arabidopsis</i>

Rieu, Ivo; Eriksson, Sven; Powers, Stephen J.; Gong, Fan; Griffiths, J.; Woolley, Lindsey; Benlloch, Reyes; Nilsson, Ove; Thomas, Stephen G.; Hedden, Peter; Phillips, Andrew L.

doi:10.1105/tpc.108.058818

Cited by 287 publications

(287 citation statements)

References 75 publications

(119 reference statements)

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“…We therefore considered gibberellin degradation to be negligible in the model. We further confirmed this model assumption by analyzing the morphology of ga2ox quintuple mutants (29), in which five of the GA2-oxidases are no longer expressed (including AtGA2ox6). Measurements of the root growth rate, elongation zone length, and cell lengths were similar to those in wild-type plants (SI Appendix, Fig.…”

Section: Resultssupporting

confidence: 51%

“…Gibberellin can also be deactivated by members of GA2-oxidase family; however, transcriptomics data for dissected regions of the root (28) revealed that the GA2-oxidase is not expressed in the elongation zone [with AtGA2ox6, the main GA2-oxidase expressed in Arabidopsis roots (29), being expressed only once the cells leave this zone]. We therefore considered gibberellin degradation to be negligible in the model.…”

Section: Resultsmentioning

confidence: 99%

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Growth-induced hormone dilution can explain the dynamics of plant root cell elongation

Band

Úbeda-Tomás

Dyson

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

103

122

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In the elongation zone of the Arabidopsis thaliana plant root, cells undergo rapid elongation, increasing their length by ∼10-fold over 5 h while maintaining a constant radius. Although progress is being made in understanding how this growth is regulated, little consideration has been given as to how cell elongation affects the distribution of the key regulating hormones. Using a multiscale mathematical model and measurements of growth dynamics, we investigate the distribution of the hormone gibberellin in the root elongation zone. The model quantifies how rapid cell expansion causes gibberellin to dilute, creating a significant gradient in gibberellin levels. By incorporating the gibberellin signaling network, we simulate how gibberellin dilution affects the downstream components, including the growth-repressing DELLA proteins. We predict a gradient in DELLA that provides an explanation of the reduction in growth exhibited as cells move toward the end of the elongation zone. These results are validated at the molecular level by comparing predicted mRNA levels with transcriptomic data. To explore the dynamics further, we simulate perturbed systems in which gibberellin levels are reduced, considering both genetically modified and chemically treated roots. By modeling these cases, we predict how these perturbations affect gibberellin and DELLA levels and thereby provide insight into their altered growth dynamics.H ormone distributions within plant tissues affect plant growth and development (1). Although many studies have investigated the influence of nonuniform distributions of the hormone auxin, gradients in other hormones also govern plant growth (2, 3). In some regions of the plant, cells undergo rapid expansion that dilutes their contents, including hormones. In these regions, organ-scale hormone gradients can arise due to the interplay between dilution, diffusion, production, decay, and receptor binding. Such complex dynamics govern in particular the distribution of the plant hormone gibberellin, which is involved in a diverse range of developmental processes including germination, organ development, and growth (4).A well-studied context for gibberellin growth regulation is provided by the primary root of the model species Arabidopsis thaliana (3, 5, 6). At the organ level, the Arabidopsis primary root classically presents three distinct morphological zones (ref. 7; Fig. 1A): Cells divide in the meristem, which is located close to the root tip; after a number of divisions, cells then move through the elongation zone, where they rapidly increase in length with negligible change in radius; finally, cells stop growing on entering the mature zone. Gibberellin has been described as a key hormone in regulating both cell division in the root meristem (6) and cell elongation in the elongation zone (5).Gibberellin regulates cell elongation and division by mediating the destabilization of DELLA proteins (8, 9). Gibberellin first binds with its receptor GID1, forming gibberellin-GID1 complexes that can then interact wi...

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Section: Resultssupporting

confidence: 51%

Section: Resultsmentioning

confidence: 99%

Growth-induced hormone dilution can explain the dynamics of plant root cell elongation

Band

Úbeda-Tomás

Dyson

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

103

122

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“…This chemical treatment was confirmed by mutant analysis. To avoid pleiotropic effects, we selected mutants with altered GA levels or DELLA activity that showed relatively limited growth phenotypes under normal conditions: q-ga2ox, a quintuple knockout for five GA 2-oxidases, resulting in higher GA levels (Rieu et al, 2008a); spy-3, a weak loss-of-function allele of the DELLA activator SPY (Jacobsen and Olszewski, 1993;Silverstone et al, 2007); the double DELLA loss-offunction mutant rga-28 gai-2; and ga3ox1-3, in which the major GA 3-oxidase responsible for GA biosynthesis in vegetative tissues is inactive, resulting in Figure 1. A, Levels of the GA biosynthesis gene GA3OX1 and the GA catabolic gene GA2OX6 at 24 h after transfer to mannitol.…”

Section: Dellas Trigger Mitotic Exitmentioning

confidence: 99%

“…The regulation of GA levels occurs at both biosynthesis, through GA 20-oxidases (GA20OX) and GA 3-oxidases (GA3OX), and degradation, which is mainly catalyzed by GA 2-oxidases (GA2OX). All these enzymes occur in small families in Arabidopsis and have tissue-specific expression patterns (Mitchum et al, 2006;Rieu et al, 2008aRieu et al, , 2008b, allowing for a tight temporal and spatial control of GA levels. GA signaling occurs by binding of GA to its receptor, GA INSENSITIVE DWARF1, leading to the formation of a complex with DELLA proteins, transcriptional regulators that inhibit GA responses in the absence of GA.…”

mentioning

confidence: 99%

DELLA Signaling Mediates Stress-Induced Cell Differentiation in Arabidopsis Leaves through Modulation of Anaphase-Promoting Complex/Cyclosome Activity

et al. 2012

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Drought is responsible for considerable yield losses in agriculture due to its detrimental effects on growth. Drought responses have been extensively studied, but mostly on the level of complete plants or mature tissues. However, stress responses were shown to be highly tissue and developmental stage specific, and dividing tissues have developed unique mechanisms to respond to stress. Previously, we studied the effects of osmotic stress on dividing leaf cells in Arabidopsis (Arabidopsis thaliana) and found that stress causes early mitotic exit, in which cells end their mitotic division and start endoreduplication earlier. In this study, we analyzed this phenomenon in more detail. Osmotic stress induces changes in gibberellin metabolism, resulting in the stabilization of DELLAs, which are responsible for mitotic exit and earlier onset of endoreduplication. Consequently, this response is absent in mutants with altered gibberellin levels or DELLA activity. Mitotic exit and onset of endoreduplication do not correlate with an up-regulation of known cell cycle inhibitors but are the result of reduced levels of DP-E2F-LIKE1/E2Fe and UV-B-INSENSITIVE4, both inhibitors of the developmental transition from mitosis to endoreduplication by modulating anaphase-promoting complex/cyclosome activity, which are down-regulated rapidly after DELLA stabilization. This work fits into an emerging view of DELLAs as regulators of cell division by regulating the transition to endoreduplication and differentiation.

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“…Upon short‐term exposure to mannitol, a gradually increasing number of genes encoding TFs is significantly upregulated, suggesting that a transcriptional cascade initiates the early response to mannitol. Few members of this transcriptional cascade have been studied previously, such as the rapidly induced ETHYLENE RESPONSE FACTOR 6 ( ERF6 ), which activates the expression of GIBBERELLIN2‐OXIDASE6 ( GA2‐OX6 ), a gene encoding a gibberellin‐inactivating enzyme (Rieu et al , 2008; Dubois et al , 2013). Because of the resulting lower levels of gibberellin, DELLA proteins are stabilized, which ensures that cells permanently exit the cell division phase and are pushed to cell differentiation (Claeys et al , 2012).…”

Section: Introductionmentioning

confidence: 99%

From network to phenotype: the dynamic wiring of an Arabidopsis transcriptional network induced by osmotic stress

Broeck

Dubois

Vermeersch

et al. 2017

Molecular Systems Biology

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Plants have established different mechanisms to cope with environmental fluctuations and accordingly fine‐tune their growth and development through the regulation of complex molecular networks. It is largely unknown how the network architectures change and what the key regulators in stress responses and plant growth are. Here, we investigated a complex, highly interconnected network of 20 Arabidopsis transcription factors (TFs) at the basis of leaf growth inhibition upon mild osmotic stress. We tracked the dynamic behavior of the stress‐responsive TFs over time, showing the rapid induction following stress treatment, specifically in growing leaves. The connections between the TFs were uncovered using inducible overexpression lines and were validated with transient expression assays. This study resulted in the identification of a core network, composed of ERF6, ERF8, ERF9, ERF59, and ERF98, which is responsible for most transcriptional connections. The analyses highlight the biological function of this core network in environmental adaptation and its redundancy. Finally, a phenotypic analysis of loss‐of‐function and gain‐of‐function lines of the transcription factors established multiple connections between the stress‐responsive network and leaf growth.

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Genetic Analysis Reveals That C19-GA 2-Oxidation Is a Major Gibberellin Inactivation Pathway inArabidopsis

Cited by 287 publications

References 75 publications

Growth-induced hormone dilution can explain the dynamics of plant root cell elongation

Growth-induced hormone dilution can explain the dynamics of plant root cell elongation

DELLA Signaling Mediates Stress-Induced Cell Differentiation in Arabidopsis Leaves through Modulation of Anaphase-Promoting Complex/Cyclosome Activity

From network to phenotype: the dynamic wiring of an Arabidopsis transcriptional network induced by osmotic stress

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