Interaction of the WD40 Domain of a Myoinositol Polyphosphate 5-Phosphatase with SnRK1 Links Inositol, Sugar, and Stress Signaling

Ananieva, Elitsa; Gillaspy, Glenda E.; Ely, Amanda; Burnette, Ryan N.; Erickson, F. Les

doi:10.1104/pp.108.130575

Cited by 82 publications

(86 citation statements)

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“…AtSnRK1 activity is repressed by inorganic phosphate starvation and trehalose-6-phosphate application (Fragoso et al, 2009;Zhang et al, 2009) and binds to myoinositol polyphosphate-5-phosphatase, which negatively regulates the kinase activity (Ananieva et al, 2008). AtSnRK1-activating kinases, AtSnAK1 and AtSnAK2, and AtSnRK1 establish a dynamic and reciprocal regulatory process though feedback phosphorylation (Shen et al, 2009;Crozet et al, 2010).…”

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Regulatory Functions of SnRK1 in Stress-Responsive Gene Expression and in Plant Growth and Development

et al. 2012

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Sucrose-nonfermentation1-related protein kinase1 (SnRK1) is an evolutionarily conserved energy sensor protein that regulates gene expression in response to energy depletion in plants. Efforts to elucidate the functions and mechanisms of this protein kinase are hampered, however, by inherent growth defects of snrk1-null mutant plants. To overcome these limitations and study SnRK1 functions in vivo, we applied a method combining transient expression in leaf mesophyll protoplasts and stable expression in transgenic plants. We found that both rice (Oryza sativa) and Arabidopsis (Arabidopsis thaliana) SnRK1 activities critically influence stress-inducible gene expression and the induction of stress tolerance. Genetic, molecular, and chromatin immunoprecipitation analyses further revealed that the nuclear SnRK1 modulated target gene transcription in a submergencedependent manner. From early seedling development through late senescence, SnRK1 activities appeared to modulate developmental processes in the plants. Our findings offer insight into the regulatory functions of plant SnRK1 in stressresponsive gene regulation and in plant growth and development throughout the life cycle.

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Regulatory Functions of SnRK1 in Stress-Responsive Gene Expression and in Plant Growth and Development

et al. 2012

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“…14 We found that loss of 5PTase13 function affects SnRK1 activity, and the impact differs depending on nutrient availability. We showed that 5ptase13 mutants contain significantly elevated SnRK1 activity in the absence of nutrients.…”

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confidence: 74%

“…16 Using the WD40 repeat region of one of the 5PTases (5PTase13), we found that 5PTase13 forms a protein complex with a sucrose (Suc) nonfermenting-1-related kinase (SnRK1.1, AKIN10; At3g01090) ) in a yeast two hybrid screen and in vitro. 14 The net result may increase myo-inositol synthesis, decrease myo-inositol oxidation, and decrease InsP 3 hydrolysis. 5PTase13 and SnRK1.1 can form a complex and under these conditions 5PTase13 protects SnRK1.1 from proteasomal destruction.…”

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“…16 Using the WD40 repeat region of one of the 5PTases (5PTase13), we found that 5PTase13 forms a protein complex with a sucrose (Suc) nonfermenting-1-related kinase (SnRK1.1, AKIN10; At3g01090) ) in a yeast two hybrid screen and in vitro. 14 Recently SnRK1.1 and its closely related isoform SnRK1.2 have been identified as central regulators of the transcriptome in response to darkness and multiple types of stress signals. 15,16 Our identification of a 5PTase13:SnRK1.1 complex Figure 1.…”

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Switches in nutrient and inositol signaling

Ananieva

Gillaspy

2009

Plant Signaling & Behavior

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Studies of signal transduction networks such as the inositol signaling pathway can provide important insights for our understanding of the regulation of various biological events, including growth and development, disease and stress responses. Recently, we have identified a myo-inositol polyphosphate 5-phosphatase (5PTase13, At1g05630) that hydrolyzes the second messenger inositol 1,4,5-trisphosphate [Ins(1,4,5)P 3 ] and also interacts with the sucrose nonfermenting-1-related kinase (SnRK1.1) in the yeast two hybrid system and in vitro. Plant SnRK1 proteins coordinate nutrient and developmental signals to regulate plant survival under stress, darkness and sugar deprivation conditions. Using mutants defective in 5PTase13, we showed that 5PTase13 can act as a regulator of SnRK1 activity, and that regulation differs with nutrient availability. Specifically, we showed that 5PTase13 acts as a positive regulator of SnRK1 activity by preventing SnRK1.1 from proteasomal degradation in the presence of low nutrients or 6% glucose. In contrast, under severe starvation conditions, 5PTase13 acts as a negative regulator of SnRK1 activity. We present here a model of 5PTase13 regulatory interaction with SnRK1.1 and further discuss its importance for balancing inositol signaling and metabolism.Phosphorylated derivatives of myo-inositol and phosphatidylinositol (PtdIns) molecules are key components with many signaling functions in plants and animals. [1][2][3][4] They are synthesized by phosphorylation of the myo-inositol ring and their metabolism is accurately regulated by diverse families of specific kinases and phosphatases. 5-7 A canonical pathway of inositol signaling involves signaling-mediated conversion of PtdIns(4,5)P 2 into diacylglycerol and Ins(1,4,5)P 3 (Fig. 1). We and others have shown that elevated Ins(1,4,5)P 3 is correlated with downstream responses to ABA and sugars. [8][9][10][11] A protein family containing 15 members of the myo-inositol polyphosphate 5-phosphatases (5PTases) terminate inositol signaling by hydrolyzing the 5-phosphates from a variety of PtdInsP and InsP substrates, including Ins(1,4,5)P 3 . 12 Four of the Arabidopsis 5PTases contain a large, N-terminal extension containing five to six WD40 repeat regions 12,13 that is capable of mediating protein-protein interactions. 16 Using the WD40 repeat region of one of the 5PTases (5PTase13), we found that 5PTase13 forms a protein complex with a sucrose (Suc) nonfermenting-1-related kinase (SnRK1.1, AKIN10; At3g01090) ) in a yeast two hybrid screen and in vitro. 14 The net result may increase myo-inositol synthesis, decrease myo-inositol oxidation, and decrease InsP 3 hydrolysis. 5PTase13 and SnRK1.1 can form a complex and under these conditions 5PTase13 protects SnRK1.1 from proteasomal destruction. Thus we propose that 5PTase13 likely regulates SnRK in a nutrient dependent manner to contribute to the fine-tuning of inositol signaling and metabolism. Abbreviations are in the text.

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“…Comprehensive analysis of global transcript levels illustrates the close link between sugar, light, and circadian responses (Usadel et al, 2008) and KIN10-regulated genes (Baena-González and Sheen, 2008). An Arabidopsis WD40 domain-containing myoinnositol polyphosphate 5-phosphase (5PTase13) directly interacts and modulates SnRK1 activity, and plays a regulatory role linking inositol, sugar, and stress signaling (Ananieva et al, 2008). The 5ptase13 mutant is Glc and ABA resistant.…”

Section: Connecting the Sugar Signaling Networkmentioning

confidence: 99%

Discover and Connect Cellular Signaling

Sheen

2010

Plant Physiology

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The unique nature of the plant system as a selfsufficient, robust, and resilient organism requires the dynamic coordination of numerous signal transduction pathways in multiple organs and cell types with complementary functions to capture energy and nutrients, to orchestrate growth and development, to adjust or adapt to fluctuating environment, and to live with symbiotic or curb invasive microbes and animals. Plants "move" through their growth and developmental programs highly integrated with the complex environmental cues. Our understanding of plant signal transduction pathways has been greatly facilitated by the isolation and characterization of a wealth of mutant collections in Arabidopsis (Arabidopsis thaliana), rice (Oryza sativa), maize (Zea mays), wheat (Triticum aestivum), barley (Hordeum vulgare), pea (Pisum sativum), tomato (Solanum lycopersicum), Medicago truncatula, moss (Physcomitrella patens), Chlamydomonas reinhardtii, and many other plants. A quantum leap in the field was made possible when the molecular cloning of mutated genes and transgenic plant analysis became a reality in several reference plants in the past two decades. Although the mainstream research on signal transduction has focused on single signals and linear pathways, recent findings have revealed many previously unexpected signaling interconnections, manifesting both the complexity and reality (Fig. 1). The increasing availability of annotated plant genome sequences and large-scale genome-wide databases and computational tools have further empowered the dissection of signaling pathways based on traditional characterization in whole plants, organs, or tissues. Moving forward to discovering and connecting the cellular signaling networks, functional characterization of thousands of genes encoding large families of key regulatory components (Fig. 1) in single cell resolution with time kinetics will be the next challenge. Integrative approaches combing creative genetics, sensitive mass spectrometry, genome-wide screens, powerful bioinformatics tools and skills, versatile cell-based assays, and targeted mutagenesis will be critical for future discoveries (Fig. 2). Glc signaling networks and emerging research tools are briefly highlighted to help pave the way for future research in cellular signaling. CONNECTING THE SUGAR SIGNALING NETWORKCharacterization of plant signaling pathways has been remarkably successful based on single signals (e.g. hormones, stresses, and microbial elicitors) and phenotypic or reporter-based observation of insensitive, constitutive, or hypersensitive response mutants, especially in Arabidopsis and rice. General frameworks, often with linear relationship of positive or negative regulators, for many plant signaling pathways have been established based on the initial signals applied in the mutant screens and molecular identification of the mutated genes. However, Arabidopsis mutant screens with an unconventional signal such as Glc (e.g. at high concentrations to trigger developmental arrest of seedlings) have reve...

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Interaction of the WD40 Domain of a Myoinositol Polyphosphate 5-Phosphatase with SnRK1 Links Inositol, Sugar, and Stress Signaling

Cited by 82 publications

References 70 publications

Regulatory Functions of SnRK1 in Stress-Responsive Gene Expression and in Plant Growth and Development

Regulatory Functions of SnRK1 in Stress-Responsive Gene Expression and in Plant Growth and Development

Switches in nutrient and inositol signaling

Discover and Connect Cellular Signaling

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