ABA‐dependent inhibition of the ubiquitin proteasome system during germination at high temperature in <i>Arabidopsis</i>

Chiu, Rex Shun; Pan, Shiyue; Zhao, Rongmin; Gazzarrini, Sonia

doi:10.1111/tpj.13293

Cited by 33 publications

(36 citation statements)

References 72 publications

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“…When GA was supplied during imbibition at 32 C, the half-life of FUS3 was shortened from 50 minutes to 15 minutes (Fig. 2B), similarly to FUS3 degradation rates at 21 C. 14 These results, together with those presented in our recent study, 14 show that inhibition of FUS3 degradation at high temperature is dependent on ABA synthesis and signaling. They also show that GA negatively regulates FUS3 levels by accelerating FUS3 degradation.…”

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confidence: 71%

“…We propose that dampening of proteasome activity may be one of the mechanisms put in place to prevent germination at supra-optimal temperature, by reducing the degradation of FUS3 and likely of other germination inhibitors, such as ABI3/ ABI5/DELLA. 14 In this study, we used a mutant affected in one of the ABA receptor family genes, the PYRABACTIN-RESISTANT 1 (PYR1), to understand if FUS3 accumulation during heat stress is dependent on ABA signaling. 15 Members of the PYR/PYL family, including PYL1, contribute to ABA sensitivity in seeds.…”

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Inhibition of FUSCA3 degradation at high temperature is dependent on ABA signaling and is regulated by the ABA/GA ratio

Chiu

Saleh

Gazzarrini

2016

Plant Signaling & Behavior

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During seed imbibition at supra-optimal temperature, an increase in the abscisic acid (ABA)/gibberellin (GA) ratio imposes secondary dormancy to prevent germination (thermoinhibition). FUSCA3 (FUS3), a positive regulator of seed dormancy, accumulates in seeds imbibed at high temperature and increases ABA levels to inhibit germination. Recently, we showed that ABA inhibits FUS3 degradation at high temperature, and that ABA and high temperature also inhibit the ubiquitin-proteasome system, by dampening both proteasome activity and protein polyubiquitination. Here, we investigated the role of ABA signaling components and the ABA antagonizing hormone, GA, in the regulation of FUS3 levels. We show that the ABA receptor mutant, pyl1-1, is less sensitive to ABA and thermoinhibition. In this mutant background, FUS3 degradation in vitro is faster. Similarly, GA alleviates thermoinhibition and also increases FUS3 degradation. These results indicate that inhibition of FUS3 degradation at high temperature is dependent on a high ABA/GA ratio and a functional ABA signaling pathway. Thus, FUS3 constitutes an important node in ABA-GA crosstalk during germination at supra-optimal temperature. KEYWORDS ABA; dormancy; FUSCA3; GA; germination; high temperature; protein degradation; proteasome; thermoinhibition; ubiquitin proteasome system; UPS Seed dormancy is an important adaptive trait that prevents seedling establishment under unfavourable conditions to maximize plant survival. Dormancy prevents pre-harvest sprouting of mature seeds and precocious germination or vivipary of immature seeds when still attached to the mother plant. These processes can lead to severe yield loss in agricultural crops. While primary dormancy is induced during seed maturation, secondary dormancy can be imposed in mature seeds with non-deep dormancy to prevent their germination under unfavourable growth conditions such as high temperature. [1][2] In Arabidopsis, the transcription factor FUSCA3 (FUS3) is essential for seed maturation and regulates several processes including the establishment of primary dormancy during embryogenesis. Loss-of-function fus3 embryos skip dormancy and can germinate precociously, while mutants ectopically expressing FUS3 post-embryonically display increased dormancy and show delayed germination, growth and flowering among several other phenotypes. 3-6 FUS3 represses developmental phase transitions by increasing the levels of the dormancy-promoting hormone, abscisic acid (ABA), while repressing the synthesis of the germination/growth-promoting hormone, gibberellin A (GA). 5,7,8 FUS3 is itself regulated by these hormones: the protein is more abundant in the presence of ABA and less abundant in the presence of GA. Exogenous GA application or reduction of endogenous ABA both partially rescue FUS3 overexpression phenotypes, such as the delayed growth, flowering and reduced cell cycling. 5 While FUS3 was shown to directly bind and repress GA biosynthetic genes, 4,8 the mechanisms behind the regulation of FUS3 protein levels...

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confidence: 71%

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confidence: 99%

Inhibition of FUSCA3 degradation at high temperature is dependent on ABA signaling and is regulated by the ABA/GA ratio

Chiu

Saleh

Gazzarrini

2016

Plant Signaling & Behavior

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“…Treatments with proteasome inhibitor were carried out as follow: after surface‐sterilization, stratification, and light‐induced germination, as described above, pHY5::HY5‐YFP hy5 hyl1‐2 seeds were grown for 1 day in darkness on 0.5 MS plates and then transferred to 0.5 MS + 50 µ m MG‐132 (Cayman Chemical, Ann Arbor, MI, USA) or + DMSO as control for and additional 1 day in darkness. Treatments were initiated on 1 dD‐grown seedlings because proteasome activity is required for germination of the seeds (Chiu et al , ).…”

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confidence: 99%

Dual function of HYPONASTIC LEAVES 1 during early skotomorphogenic growth in Arabidopsis

et al. 2020

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Seeds germinating underground display a specific developmental programme, termed skotomorphogenesis, to ensure survival of the emerging seedlings until they reach the light. They rapidly elongate the hypocotyl and maintain the cotyledons closed, forming a hook with the hypocotyl in order to protect apical meristematic cells from mechanical damage. Such crucial events for the fate of the seedling are tightly regulated and although some transcriptional regulators and phytohormones are known to be implicated in this regulation, we are still far from a complete understanding of these biological processes. Our work provides information on the diverse roles in skotomorphogenesis of the core components of microRNA biogenesis in Arabidopsis, HYL1, DCL1, and SE. We show that hypocotyl elongation is promoted by all these components, probably through the action of specific miRNAs. Hook development also depends on these proteins however, remarkably, HYL1 exerts its role in an opposite way to DCL1 and SE. Interestingly, we found that a specific HYL1 domain involved in protein-protein interaction is required for this function. Genetic evidences also point to the phosphorylation status of HYL1 as important for this function. We propose that HYL1 help maintain the hook closed during early skotomorphogenesis in a microprocessor-independent manner by repressing the activity of HY5, the transcriptional master regulator that triggers light responses. This work uncovers a previously unnoticed link between components of the miRNA biogenesis machinery, the skotomorphogenic growth, and hook development in Arabidopsis.Plasmids containing pHYL1::HYL1-CFP and pSE::YFP-SE (Fang and Spector, 2007) used for transformation of hyl1-2 or se-1 plants, respectively, were a kind gift from Dr Fang and Dr Spector. Agrobacterium tumefaciens strain GV3101 containing each construct with the respective translational fusion under the

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“…For example, in Arabidopsis , high temperature inhibited the function of the ubiquitin proteasome system, but the inhibition was reduced in ABA biosynthetic mutants and in plants by the treatment of fluridone (ABA biosynthesis inhibitor), suggesting that it was regulated by high temperature in an ABA-dependent manner (Chiu et al, 2016). In Physcomitrella patens , the accumulation of low-molecular-weight soluble (LMS) sugars had no significant effect on the ABA-deficient mutant ppaba1 and its wild type after hyperosmotic and ABA treatments, suggesting that LMS sugars were regulated by hyperosmotic stress in an ABA-independent way (Takezawa et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Quantitative Proteomic Analyses Identify ABA-Related Proteins and Signal Pathways in Maize Leaves under Drought Conditions

et al. 2016

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Drought stress is one of major factors resulting in maize yield loss. The roles of abscisic acid (ABA) have been widely studied in crops in response to drought stress. However, more attention is needed to identify key ABA-related proteins and also gain deeper molecular insights about drought stress in maize. Based on this need, the physiology and proteomics of the ABA-deficient maize mutant vp5 and its wild-type Vp5 under drought stress were examined and analyzed. Malondialdehyde content increased and quantum efficiency of photosystem II decreased under drought stress in both genotypes. However, the magnitude of the increase or decrease was significantly higher in vp5 than in Vp5. A total of 7051 proteins with overlapping expression patterns among three replicates in the two genotypes were identified by Multiplex run iTRAQ-based quantitative proteomic and liquid chromatography-tandem mass spectrometry methods, of which the expression of only 150 proteins (130 in Vp5, 27 in vp5) showed changes of at least 1.5-fold under drought stress. Among the 150 proteins, 67 and 60 proteins were up-regulated and down-regulated by drought stress in an ABA-dependent way, respectively. ABA was found to play active roles in regulating signaling pathways related to photosynthesis, oxidative phosphorylation (mainly related to ATP synthesis), and glutathione metabolism (involved in antioxidative reaction) in the maize response to drought stress. Our results provide an extensive dataset of ABA-dependent, drought-regulated proteins in maize plants, which may help to elucidate the underlying mechanisms of ABA-enhanced tolerance to drought stress in maize.

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ABA‐dependent inhibition of the ubiquitin proteasome system during germination at high temperature in Arabidopsis

Cited by 33 publications

References 72 publications

Inhibition of FUSCA3 degradation at high temperature is dependent on ABA signaling and is regulated by the ABA/GA ratio

Inhibition of FUSCA3 degradation at high temperature is dependent on ABA signaling and is regulated by the ABA/GA ratio

Dual function of HYPONASTIC LEAVES 1 during early skotomorphogenic growth in Arabidopsis

Quantitative Proteomic Analyses Identify ABA-Related Proteins and Signal Pathways in Maize Leaves under Drought Conditions

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