The Arabidopsis <i>GSQ5/DOG1</i> Cvi allele is induced by the ABA‐mediated sugar signalling pathway, and enhances sugar sensitivity by stimulating <i>ABI4</i> expression

Teng, Sheng; Rognoni, Sara; Bentsink, Leónie; Smeekens, Sjef

doi:10.1111/j.1365-313x.2008.03515.x

Cited by 57 publications

(44 citation statements)

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“…Comparison of the fructose-sensitivity QTLs with those published previously for glucose sensing (23) in the same population showed that FSQ3, FSQ4, FSQ6, and FSQ8 are fructose specific. Among these, the fructose sensitivity of FSQ6 had the highest LOD score and was confirmed using the NIL line LCN5-7.…”

Section: Resultsmentioning

confidence: 91%

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Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain

Wind

Shi

et al. 2011

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

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115

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In living organisms sugars not only provide energy and carbon skeletons but also act as evolutionarily conserved signaling molecules. The three major soluble sugars in plants are sucrose, glucose, and fructose. Information on plant glucose and sucrose signaling is available, but to date no fructose-specific signaling pathway has been reported. In this study, sugar repression of seedling development was used to study fructose sensitivity in the Landsberg erecta (Ler)/Cape Verde Islands (Cvi) recombinant inbred line population, and eight fructose-sensing quantitative trait loci (QTLs) (FSQ1-8) were mapped. Among them, FSQ6 was confirmed to be a fructose-specific QTL by analyzing near-isogenic lines in which Cvi genomic fragments were introgressed in the Ler background. These results indicate the existence of a fructose-specific signaling pathway in Arabidopsis. Further analysis demonstrated that the FSQ6-associated fructose-signaling pathway functions independently of the hexokinase1 (HXK1) glucose sensor. Remarkably, fructosespecific FSQ6 downstream signaling interacts with abscisic acid (ABA)-and ethylene-signaling pathways, similar to HXK1-dependent glucose signaling. The Cvi allele of FSQ6 acts as a suppressor of fructose signaling. The FSQ6 gene was identified using mapbased cloning approach, and FSQ6 was shown to encode the transcription factor gene Arabidopsis NAC (petunia No apical meristem and Arabidopsis transcription activation factor 1, 2 and Cup-shaped cotyledon 2) domain containing protein 89 (ANAC089). The Cvi allele of FSQ6/ANAC089 is a gain-of-function allele caused by a premature stop in the third exon of the gene. The truncated Cvi FSQ6/ ANAC089 protein lacks a membrane association domain that is present in ANAC089 proteins from other Arabidopsis accessions. As a result, Cvi FSQ6/ANAC089 is constitutively active as a transcription factor in the nucleus. I n plants, sugars provide the energy and carbon skeletons needed for growth and in addition act as crucial signaling molecules that affect growth, development, and response to the (a)biotic environment (1-3). Plant cells harbor sugar-sensing and -signaling systems that regulate the expression of thousands of genes and control the metabolic processes needed for growth (2-4). These sugar-response systems are known to interact with other signaling pathways, such as those for light, phytohormones, stress, and nutrients (1).The neutral sugars sucrose, glucose, and fructose are central to metabolism in plants and in other organisms as well. So far, detailed information is available only on glucose sensing, and it has been shown that the hexokinase 1 (HXK1) enzyme acts as a glucose sensor (5, 6). Sucrose-specific signaling also was demonstrated because the effect of sucrose cannot be mimicked by glucose and/or fructose (7), but so far no information on sucrosesensing systems is available. A signaling function for fructose has been proposed (8, 9), but no convincing experimental evidence on such fructose-specific signaling is available.In Arabidopsis ea...

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Section: Resultsmentioning

confidence: 91%

“…QTL analysis was performed using MapQTL as described (23,38). FSQ6 initially was mapped between T6G21 and K8E10 in 113 fully arrested F 2 individuals derived from the crossing between LCN5-7 and Ler.…”

Section: Methodsmentioning

confidence: 99%

Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain

Wind

Shi

et al. 2011

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

Self Cite

115

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“…S4). DOG1 is the gene at the loci with the strongest dormancy association in QTL analyses (20), and its expression, although not directly associated with ABA, is altered by environmental conditions (22) and may enhance ABA sensitivity (23). MFT, a homolog of the antagonistic flowering-time regulators FLOWERING LOCUS T (FT) and TERMINAL FLOWER 1 (TFL1) is a proposed ABA-induced negative regulator of ABA signaling that promotes embryo growth in germinating seeds (19).…”

Section: Resultsmentioning

confidence: 99%

Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways

Footitt

Douterelo-Soler

Clay

et al. 2011

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

280

402

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Seeds respond to environmental signals, tuning their dormancy cycles to the seasons and thereby determining the optimum time for plant establishment. The molecular regulation of dormancy cycling is unknown, but an extensive range of mechanisms have been identified in laboratory experiments. Using a targeted investigation of gene expression over the dormancy cycle of Arabidopsis seeds in the field, we investigated how these mechanisms are seasonally coordinated. Depth of dormancy and gene expression patterns were correlated with seasonal changes in soil temperature. The results were consistent with abscisic acid (ABA) signaling linked to deep dormancy in winter being repressed in spring concurrent with enhanced DELLA repression of germination as depth of dormancy decreased. Dormancy increased during winter as soil temperature declined and expression of ABA synthesis (NCED6) and gibberellic acid (GA) catabolism (GA2ox2) genes increased. This was linked to an increase in endogenous ABA that plateaus, but dormancy and DOG1 and MFT expression continued to increase. The expression of SNF1-related protein kinases, SnrK 2.1 and 2.4, also increased consistent with enhanced ABA signaling and sensitivity being modulated by seasonal soil temperature. Dormancy then declined in spring and summer. Endogenous ABA decreased along with positive ABA signaling as expression of ABI2, ABI4, and ABA catabolism (CYP707A2) and GA synthesis (GA3ox1) genes increased. However, during the lowdormancy phase in the summer, expression of transcripts for the germination repressors RGA and RGL2 increased. Unlike deep winter dormancy, this represson can be removed on exposure to light, enabling the completion of germination at the correct time of year.environmental signaling | environmental sensing | seed ecology | soil seed bank S eeds are the mobile phase of the plant's life cycle; vegetative development is suspended as seeds transport the plant's genetic complement through space and time. This is achieved by a seed remaining dormant, potentially for many years/decades in the soil, until conditions occur that are suitable for the resulting plant to survive, be competitive, and reproduce. Field observations by seed ecologists show that seeds act as environmental sensors and adjust their depth of dormancy in response to a range of signals (1). Some signals (e.g., soil temperature and moisture) are related to slow seasonal change that indicates when a suitable time of year and climate space exists (temporal window). These signals are integrated over time to alter the depth of dormancy and therefore the sensitivity to a second set of signals (e.g., light, nitrate, alternating temperatures). This second set of signals indicates in a more immediate way that conditions are suitable to terminate dormancy and induce the completion of germination (spatial window: appropriate soil depth, temperature, and moisture and lack of competing plants). If the correct spatial window does not occur, the temporal window will close for another year.Despite the obvious...

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“…For example, we are learning of regulatory mechanisms that coordinate ABA vs. GA antagonisms mediating seed responses to light, chilling, and water availability via crossregulation of multiple transcription factors and their target genes (131), Studies of cross-talk with sugar signaling have identified cross-regulation of transport and metabolism, with transcription factors such as ABI4 acting as nodes (reviewed in {Gibson, 2004 #240; Dekkers, 2008 #241; (158). As more specific factors are tested genetically, and network modeling strategies are applied, our understanding of these linkages should continue to improve.…”

Section: Cross-talk With Other Signaling Pathwaysmentioning

confidence: 99%

Abscisic Acid: Emergence of a Core Signaling Network

Cutler

Rodriguez

Finkelstein

et al. 2010

Annu. Rev. Plant Biol.

2,577

2,022

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Key TermsBiFC: Bimolecular fluorescence complementation; a method for monitoring in vivo protein interactions by formation of a functional fluorescent protein DELLA: family of proteins that function as negative regulators of GA signaling, and are destabilized by GA infrared thermography: method for viewing infrared light emitted by objects due to their thermal condition; excessive transpiration results in "cool" leaves osmocompatible solutes: small molecules accumulated by cells to permit osmotic adjustment to a dehydrating environment without interfering with cellular function pyrabactin: a selective ABA agonist that is not an ABA analog Abstract Abscisic acid regulates numerous developmental processes and adaptive stress responses in plants. Many ABA signaling components have been identified, but their interconnections and a consensus on the structure of the ABA signaling network have eluded researchers. Recently, several advances have led to both the identification of ABA receptors and an understanding of how key regulatory phosphatase and kinase activities are controlled by ABA. A new model for ABA action has been proposed in which the soluble PYR/PYL/RCAR receptors function at the apex of a negative regulatory pathway to directly regulate PP2C phosphatases, which in turn directly regulate SnRK2 kinases. This model unifies many previously defined signaling components and highlights the importance of future work focused on defining the direct targets of SnRK2s and PP2Cs, dissecting the mechanisms of hormone interactions (i.e. cross-talk) and defining connections between additional known signaling components and this pathway, and determining how many other pathways control ABA signaling.Abscisic Acid: A brief history ABA was discovered in the 1960s. Reviews of its discovery and early chemistry and biology were published in 1969 and 1974 (2, 105). Briefly, ABA was isolated by several groups using activity-guided purification approaches to isolate endogenous growth regulators. Addicott's group at the USDA was searching for compounds isolated from cotton that promote leaf abscission, using a cotyledon abscission assay to guide purification (122). The compound isolated, originally named abscisin II, was also determined to inhibit Avena coleoptile growth (122). ABA's abscission promoting effect was subsequently determined to be partly an indirect consequence of inducing ethylene biosynthesis (26). The Wareing and Cornforth groups in the UK searched for compounds that promote bud dormancy, reasoned that such compounds would be general growth inhibitors, and ultimately isolated dormin as a wheat embryo germination inhibitor present in sycamore leaf extracts. Chemical analyses showed dormin and abscisin II to be the same compound (25), which was ultimately renamed abscisic acid. A third growth inhibitory activity originally isolated from Aegopodium tubers in the 1950s and named -inhibitor (8) was also determined to be ABA (104); thus, the widespread occurrence and importance of ABA as a plant growth regulator was esta...

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The Arabidopsis GSQ5/DOG1 Cvi allele is induced by the ABA‐mediated sugar signalling pathway, and enhances sugar sensitivity by stimulating ABI4 expression

Cited by 57 publications

References 57 publications

Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain

Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain

Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways

Abscisic Acid: Emergence of a Core Signaling Network

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