Phosphorylation of WRINKLED1 by KIN10 Results in Its Proteasomal Degradation, Providing a Link between Energy Homeostasis and Lipid Biosynthesis

Zhai, Zhiyang; Liu, Hui; Shanklin, John

doi:10.1105/tpc.17.00019

Cited by 119 publications

(147 citation statements)

References 60 publications

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“…That WRI1 expression did not differ significantly between adg1suc2 and the wild type supports this view. The data presented here, that elevated sugar correlates with increased accumulation of WRI1, is consistent with the previously proposed model of WRI1 stabilization upon Suc-mediated inhibition of KIN10 (Zhai et al, 2017). This also supports our model for a dual role for sugar in providing carbon skeletons for FA synthesis and through inhibiting KIN10 activity and, thereby, stabilizing WRI1.…”

Section: Suc Favors Tag Biosynthesissupporting

confidence: 80%

“…Increased levels of sugar correlated with increased accumulation of total FA and TAG along with increased rates of FA synthesis. This likely results from a combination of two mechanisms: (1) through increasing the supply of carbon skeletons, ATP, and reductant (Sanjaya et al, 2011); and (2) via inhibiting the KIN10-dependent degradation of WRI1 (Zhai et al, 2017). Relative to the wild type, the adg1suc2 double mutant accumulated more than 80-fold higher leaf sugar, 10-fold more TAG, and substantially higher levels of WRI1.…”

Section: Resultsmentioning

confidence: 99%

“…We recently reported a mechanistic explanation for the sugar potentiation of WRI1 (i.e. that SnRK1, encoded by KIN10 and KIN11 in Arabidopsis [Williams et al, 2014], phosphorylates two previously unidentified SnRK1 target sites within WRI1 that marks it for proteasomal degradation [Zhai et al, 2017]). According to the model, under low-sugar conditions, when SnRK1 is active, WRI1 is degraded and lipid synthesis is repressed.…”

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confidence: 99%

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Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation

Zhai

Liu

et al. 2017

Plant Physiol.

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Photosynthetically derived sugar provides carbon skeletons for lipid biosynthesis. We used mutants of Arabidopsis (Arabidopsis thaliana) and the expression of oleogenic factors to investigate relationships among sugar availability, lipid synthesis, and the accumulation of triacylglycerol (TAG) in leaf tissue. The adg1 mutation disables the small subunit of ADP-glucose pyrophosphorylase, the first step in starch synthesis, and the suc2 mutation disables a sucrose/proton symporter that facilitates sucrose loading from leaves into phloem. The adg1suc2 double mutant increases glucose plus sucrose content in leaves 80-fold relative to the wild type, total fatty acid (FA) content 1.8-fold to 8.3% dry weight, and TAG more than 10-fold to 1.2% dry weight. The WRINKLED1 transcription factor also accumulates to higher levels in these leaves, and the rate of FA synthesis increases by 58%. Adding tt4, which disables chalcone synthase, had little effect, but adding the tgd1 mutation, which disables an importer of lipids into plastids to create adg1suc2tt4tgd1, increased total leaf FA to 13.5% dry weight and TAG to 3.8% dry weight, demonstrating a synergistic effect upon combining these mutations. Combining adg1suc2 with the sdp1 mutation, deficient in the predominant TAG lipase, had little effect on total FA content but increased the TAG accumulation by 66% to 2% dry weight. Expression of the WRINKLED1 transcription factor, along with DIACYLGLYCEROL ACYLTRANSFERASE1 and the OLEOSIN1 oil body-associated protein, in the adg1suc2 mutant doubled leaf FA content and increased TAG content to 2.3% dry weight, a level 4.6-fold higher than that resulting from expression of the same factors in the wild type.

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Section: Suc Favors Tag Biosynthesissupporting

confidence: 80%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation

Zhai

Liu

et al. 2017

Plant Physiol.

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“…WRI1 also is a positive regulator of glycolysis and lipid biosynthesis in Arabidopsis, and recently, phosphorylation of WRI1 by AKIN10 was shown to result in its proteasomal degradation (Zhai et al, 2017). This AKIN10-dependent degradation of WRI1 provides a homeostatic mechanism that favors lipid biosynthesis when intracellular sugar levels are elevated and AKIN10 is inhibited.…”

Section: Anterograde Signals To Organelles Via Phosphorylation Of Tramentioning

confidence: 99%

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

et al. 2018

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The evolutionarily conserved SNF1-related protein kinase 1 (SnRK1) kinase complex is a key regulator in adjusting cellular metabolism during starvation, stress conditions, and growth-promoting conditions. Over the last two decades, extensive genetic evidence for a widespread SnRK1 signaling network has accumulated. It is now well established that SnRK1 is a central integrator of energy signaling. However, little is known about the connections between the cytoplasmic and nuclear-localized SnRK1 and plastids and mitochondria as the main energy-producing compartments in the cell. Here, we review recent findings indicating how SnRK1 affects metabolic adaptation, including plastidial and mitochondrial functions. Special emphasis is put on identified direct targets of SnRK1, which would eventually enable cross talk with organelles. In this context, a number of transcription factors (TFs) are emerging as mediators of SnRK1 signaling, potentially linking SnRK1 activity to organellar functions. Furthermore, many SnRK1 targets act in various hormonal signaling pathways, which are at least partly localized in plastids. With this review, we summarize the current knowledge on SnRK1 organelle interaction and provide ideas on the potential molecular mechanisms governing these interactions. METABOLIC REPROGRAMMING BY SNRK1 KINASE ACTIVITY UNDER DIFFERENT GROWTH AND STRESS CONDITIONSAlready under optimal growth conditions, plants need to continuously adjust their metabolic balance between autotrophic growth based on photosynthesis during the day and respiration during the night. At daytime, sugars and other metabolites are produced by photosynthesis in chloroplasts and further distributed to be used in other metabolic pathways at different cellular compartments or transported to nonphotosynthetic sink tissues. During the night, starch and sugars supply carbon equivalents for respiration, providing the necessary energy for further growth and metabolic activities. Additionally, metabolic reprogramming is required for plants to adjust their metabolism to diverse biotic and abiotic environmental stimuli. This often leads to a stop of plant growth involving a reduction in ribosomal protein synthesis, and in parallel, accumulation of protective metabolites or defense compounds. This switching of cellular energy metabolism is mediated by the activity of the evolutionarily conserved AMPK/ SNF1/SnRK1 kinase complex (Box 1; Crozet et al.,

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“…In general, SnRK1-mediated transcriptional reprogramming results in the downregulation of energy-consuming processes and the induction of catabolic pathways to provide alternative energy sources. Although the broad effect on transcription and the specificity that is required to respond to a particular stress are likely to require modulation of a range of different downstream target proteins, only a few transcription factors representing potential direct SnRK1 substrates have been identified (Kleinow et al, 2009;Tsai and Gazzarrini, 2012;Jeong et al, 2015;O'Brien et al, 2015;Zhai et al, 2017). Recently, Mair et al (2015) identified the Arabidopsis transcription factor bZIP63 as a key regulator of the starvation response and a direct target of the SnRK1 kinase.…”

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confidence: 99%

STOREKEEPER RELATED1/G-Element Binding Protein (STKR1) Interacts with Protein Kinase SnRK1

et al. 2017

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Sucrose nonfermenting related kinase1 (SnRK1) is a conserved energy sensor kinase that regulates cellular adaptation to energy deficit in plants. Activation of SnRK1 leads to the down-regulation of ATP-consuming biosynthetic processes and the stimulation of energy-generating catabolic reactions by transcriptional reprogramming and posttranslational modifications. Although considerable progress has been made during the last years in understanding the SnRK1 signaling pathway, many of its components remain unidentified. Here, we show that the catalytic a-subunits KIN10 and KIN11 of the Arabidopsis (Arabidopsis thaliana) SnRK1 complex interact with the STOREKEEPER RELATED1/G-Element Binding Protein (STKR1) inside the plant cell nucleus. Overexpression of STKR1 in transgenic Arabidopsis plants led to reduced growth, a delay in flowering, and strongly attenuated senescence. Metabolite profiling revealed that the transgenic lines exhausted their carbohydrates during the dark period to a greater extent than the wild type and accumulated a range of amino acids. At the global transcriptome level, genes affected by STKR1 overexpression were broadly associated with systemic acquired resistance, and transgenic plants showed enhanced resistance toward a virulent strain of the biotrophic oomycete pathogen Hyaloperonospora arabidopsidis Noco2. We discuss a possible connection of STKR1 function, SnRK1 signaling, and plant immunity.Plants are the prime example of photoautotrophic organisms, using photosynthesis to harness energy from sunlight for the conversion of CO 2 into energyrich carbohydrates. These photoassimilates are then directed to fuel plant growth and development. However, as sessile organisms, plants usually have to cope with strongly fluctuating environmental conditions, many of which negatively impact on energy availability, as they interfere with the production or distribution of photoassimilates. In order to maintain energy homeostasis and to promote survival, energy shortage triggers a massive cellular reprogramming characterized by nutrient remobilization, suppression of biosynthetic processes, and growth arrest (Baena-González, 2010). A central component of low-energy signaling in plants is the sucrose nonfermenting related kinase1 (SnRK1), which is orthologous to the AMP-dependent kinase (AMPK) and sucrose nonfermenting1 (SNF1) in mammals and yeast, respectively. Similar to its opisthokont counterparts, the SnRK1 holoenzyme is a heterotrimeric complex consisting of a catalytic a-subunit and noncatalytic b-and plant-specific bg-subunits (Ramon et al., 2013;Emanuelle et al., 2015). In Arabidopsis (Arabidopsis thaliana), the catalytic a-subunit is represented by two isoforms, SnRK1a1 (AKIN10; At3g01090) and SnRK1a2 (AKIN11; At3g29160), both of which appear to be expressed ubiquitously, although KIN10 accounts for the majority of SnRK1 activity (Jossier et al., 2009). Activation of SnRK1 involves the phosphorylation/ dephosphorylation of a T-loop Thr (Thr-172 of Arabidopsis SnRK1.1a) involving the upstream kinas...

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Phosphorylation of WRINKLED1 by KIN10 Results in Its Proteasomal Degradation, Providing a Link between Energy Homeostasis and Lipid Biosynthesis

Cited by 119 publications

References 60 publications

Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation

Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

STOREKEEPER RELATED1/G-Element Binding Protein (STKR1) Interacts with Protein Kinase SnRK1

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