SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana

Soto-Burgos, Junmarie; Bassham, Diane C.

doi:10.1371/journal.pone.0182591

Title: SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana

Journal Article · Fri Aug 04 00:00:00 EDT 2017 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0182591· OSTI ID:1373990

Soto-Burgos, Junmarie ^[1];

^[2]

Iowa State Univ., Ames, IA (United States). Dept. of Genetics, Development, and Cell Biology
Iowa State Univ., Ames, IA (United States). Dept. of Genetics, Development, and Cell Biology and Plant Sciences Inst.

Autophagy is a degradation process in which cells break down and recycle their cytoplasmic contents when subjected to environmental stress or during cellular remodeling. The Arabidopsis thaliana SnRK1 complex is a protein kinase that senses changes in energy levels and triggers downstream responses to enable survival. Its mammalian ortholog, AMPK, and yeast ortholog, Snf-1, activate autophagy in response to low energy conditions. We therefore hypothesized that SnRK1 may play a role in the regulation of autophagy in response to nutrient or energy deficiency in Arabidopsis. To test this hypothesis, we determined the effect of overexpression or knockout of the SnRK1 catalytic subunit KIN10 on autophagy activation by abiotic stresses, including nutrient deficiency, salt, osmotic, oxidative, and ER stress. While wild-type plants had low basal autophagy activity in control conditions, KIN10 overexpression lines had increased autophagy under these conditions, indicating activation of autophagy by SnRK1. A kin10 mutant had a basal level of autophagy under control conditions similar to wild-type plants, but activation of autophagy by most abiotic stresses was blocked, indicating that SnRK1 is required for autophagy induction by a wide variety of stress conditions. In mammals, TOR is a negative regulator of autophagy, and AMPK acts to activate autophagy both upstream of TOR, by inhibiting its activity, and in a parallel pathway. Inhibition of Arabidopsis TOR leads to activation of autophagy; inhibition of SnRK1 did not block this activation. Furthermore, an increase in SnRK1 activity was unable to induce autophagy when TOR was also activated. The results presented here demonstrate that SnRK1 acts upstream of TOR in the activation of autophagy in Arabidopsis.

View Journal Article

Cite

Export

Save

Research Organization:: Iowa State Univ., Ames, IA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0014038

OSTI ID:: 1373990

Alternate ID(s):: OSTI ID: 1425736

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Vol. 12 Journal Issue: 8; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 122 works

Citation information provided by
Web of Science

References (72)

TOR Is a Negative Regulator of Autophagy in Arabidopsis thaliana Liu, Yimo; Bassham, Diane C. PLoS ONE, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pone.0011883	journal	July 2010
The ATG1/ATG13 Protein Kinase Complex Is Both a Regulator and a Target of Autophagic Recycling in Arabidopsis Suttangkakul, Anongpat; Li, Faqiang; Chung, Taijoon The Plant Cell, Vol. 23, Issue 10 https://doi.org/10.1105/tpc.111.090993	journal	October 2011
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J. Science, Vol. 301, Issue 5633, p. 653-657 https://doi.org/10.1126/science.1086391	journal	August 2003
Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases Crozet, Pierre; Margalha, Leonor; Confraria, Ana Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00190	journal	May 2014
Tor, a Phosphatidylinositol Kinase Homologue, Controls Autophagy in Yeast Noda, Takeshi; Ohsumi, Yoshinori Journal of Biological Chemistry, Vol. 273, Issue 7 https://doi.org/10.1074/jbc.273.7.3963	journal	February 1998
Degradation of the Endoplasmic Reticulum by Autophagy during Endoplasmic Reticulum Stress in Arabidopsis Liu, Yimo; Burgos, Junmarie Soto; Deng, Yan The Plant Cell, Vol. 24, Issue 11 https://doi.org/10.1105/tpc.112.101535	journal	November 2012
Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose Harthill, Jean E.; Meek, Sarah E. M.; Morrice, Nick The Plant Journal, Vol. 47, Issue 2 https://doi.org/10.1111/j.1365-313X.2006.02780.x	journal	July 2006
SnRK1 from Arabidopsis thaliana is an atypical AMPK Emanuelle, Shane; Hossain, Mohammed Iqbal; Moller, Isabel E. The Plant Journal, Vol. 82, Issue 2 https://doi.org/10.1111/tpj.12813	journal	April 2015
An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development Deprost, Dorothée; Truong, Hoai-Nam; Robaglia, Christophe Biochemical and Biophysical Research Communications, Vol. 326, Issue 4 https://doi.org/10.1016/j.bbrc.2004.11.117	journal	January 2005
5′-AMP Activates the AMP-activated Protein Kinase Cascade, and Ca ²⁺ /Calmodulin Activates the Calmodulin-dependent Protein Kinase I Cascade, via Three Independent Mechanisms Hawley, Simon A.; Selbert, Michele A.; Goldstein, Elaine G. Journal of Biological Chemistry, Vol. 270, Issue 45 https://doi.org/10.1074/jbc.270.45.27186	journal	November 1995
The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation Deprost, Dorothée; Yao, Lei; Sormani, Rodnay EMBO reports, Vol. 8, Issue 9 https://doi.org/10.1038/sj.embor.7401043	journal	August 2007
SnRK1 Isoforms AKIN10 and AKIN11 Are Differentially Regulated in Arabidopsis Plants under Phosphate Starvation Fragoso, Selene; Espíndola, Laura; Páez-Valencia, Julio Plant Physiology, Vol. 149, Issue 4 https://doi.org/10.1104/pp.108.133298	journal	February 2009
SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana Jossier, Mathieu; Bouly, Jean-Pierre; Meimoun, Patrice The Plant Journal, Vol. 59, Issue 2 https://doi.org/10.1111/j.1365-313X.2009.03871.x	journal	July 2009
A critical role of autophagy in plant resistance to necrotrophic fungal pathogens: Autophagy in plant disease resistance Lai, Zhibing; Wang, Fei; Zheng, Zuyu The Plant Journal, Vol. 66, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04553.x	journal	April 2011
The hybrid Four-CBS-Domain KINβγ subunit functions as the canonical γ subunit of the plant energy sensor SnRK1 Ramon, Matthew; Ruelens, Philip; Li, Yi The Plant Journal, Vol. 75, Issue 1 https://doi.org/10.1111/tpj.12192	journal	May 2013
Evidence for autophagy-dependent pathways of rRNA turnover in Arabidopsis Floyd, Brice E.; Morriss, Stephanie C.; MacIntosh, Gustavo C. Autophagy, Vol. 11, Issue 12 https://doi.org/10.1080/15548627.2015.1106664	journal	December 2015
Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phosphate dynamics: PTEN regulates autophagy in pollen tubes via PI3P Zhang, Yan; Li, Sha; Zhou, Liang-Zi The Plant Journal, Vol. 68, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04761.x	journal	October 2011
Abscisic acid Biosynthesis and Catabolism Nambara, Eiji; Marion-Poll, Annie Annual Review of Plant Biology, Vol. 56, Issue 1 https://doi.org/10.1146/annurev.arplant.56.032604.144046	journal	June 2005
The Association of AMPK with ULK1 Regulates Autophagy Lee, Jong Woo; Park, Sungman; Takahashi, Yoshinori PLoS ONE, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pone.0015394	journal	November 2010
The lysosome: a crucial hub for AMPK and mTORC1 signalling Carroll, Bernadette; Dunlop, Elaine A. Biochemical Journal, Vol. 474, Issue 9 https://doi.org/10.1042/BCJ20160780	journal	April 2017
Phosphorylation of ULK1 (hATG1) by AMP-Activated Protein Kinase Connects Energy Sensing to Mitophagy Egan, D. F.; Shackelford, D. B.; Mihaylova, M. M. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1196371	journal	December 2010
Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants Chinnusamy, V. Journal of Experimental Botany, Vol. 55, Issue 395 https://doi.org/10.1093/jxb/erh005	journal	November 2003
Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase Halford, N. G.; Hey, S.; Jhurreea, D. Journal of Experimental Botany, Vol. 54, Issue 382 https://doi.org/10.1093/jxb/erg038	journal	January 2003
The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation: Regulation of AMPK/SNF1/SnRK1 kinase complexes Ghillebert, Ruben; Swinnen, Erwin; Wen, Jing FEBS Journal, Vol. 278, Issue 21 https://doi.org/10.1111/j.1742-4658.2011.08315.x	journal	September 2011
Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis Dong, Pan; Xiong, Fangjie; Que, Yumei Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00677	journal	September 2015
Mutations in the Arabidopsis Homolog of LST8/GβL, a Partner of the Target of Rapamycin Kinase, Impair Plant Growth, Flowering, and Metabolic Adaptation to Long Days Moreau, Manon; Azzopardi, Marianne; Clément, Gilles The Plant Cell, Vol. 24, Issue 2 https://doi.org/10.1105/tpc.111.091306	journal	February 2012
Mathematical modeling reveals that metabolic feedback regulation of SnRK1 and hexokinase is sufficient to control sugar homeostasis from energy depletion to full recovery NÃ¤gele, Thomas; Weckwerth, Wolfram Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00365	journal	July 2014
Regulation of Sucrose non-Fermenting Related Kinase 1 genes in Arabidopsis thaliana Williams, Sarah P.; Rangarajan, Padma; Donahue, Janet L. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00324	journal	July 2014
Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae Tsukada, Miki; Ohsumi, Yoshinori FEBS Letters, Vol. 333, Issue 1-2 https://doi.org/10.1016/0014-5793(93)80398-E	journal	October 1993
Regulation of spinach SNF1-related (SnRK1) kinases by protein kinases and phosphatases is associated with phosphorylation of the T loop and is regulated by 5'-AMP Sugden, Chris; Crawford, Russell M.; Halford, Nigel G. The Plant Journal, Vol. 19, Issue 4 https://doi.org/10.1046/j.1365-313X.1999.00532.x	journal	August 1999
AKIN βγ Contributes to SnRK1 Heterotrimeric Complexes and Interacts with Two Proteins Implicated in Plant Pathogen Resistance through Its KIS/GBD Sequence Gissot, Lionel; Polge, Cécile; Jossier, Mathieu Plant Physiology, Vol. 142, Issue 3 https://doi.org/10.1104/pp.106.087718	journal	October 2006
Atg9 Cycles Between Mitochondria and the Pre-Autophagosomal Structure in Yeasts Reggiori, Fulvio; Shintani, Takahiro; Chong, Huira Autophagy, Vol. 1, Issue 2 https://doi.org/10.4161/auto.1.2.1840	journal	July 2005
Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway Harding, T. M. The Journal of Cell Biology, Vol. 131, Issue 3 https://doi.org/10.1083/jcb.131.3.591	journal	November 1995
Antisense SNF1-related (SnRK1) protein kinase gene represses transient activity of an alpha-amylase (alpha-Amy2) gene promoter in cultured wheat embryos Laurie, S. Journal of Experimental Botany, Vol. 54, Issue 383 https://doi.org/10.1093/jxb/erg085	journal	February 2003
-Subunit myristoylation is the gatekeeper for initiating metabolic stress sensing by AMP-activated protein kinase (AMPK) Oakhill, J. S.; Chen, Z. -P.; Scott, J. W. Proceedings of the National Academy of Sciences, Vol. 107, Issue 45 https://doi.org/10.1073/pnas.1009705107	journal	October 2010
AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1 Kim, Joungmok; Kundu, Mondira; Viollet, Benoit Nature Cell Biology, Vol. 13, Issue 2 https://doi.org/10.1038/ncb2152	journal	January 2011
AMP-activated protein kinase--an energy sensor that regulates all aspects of cell function Hardie, D. G. Genes & Development, Vol. 25, Issue 18 https://doi.org/10.1101/gad.17420111	journal	September 2011
Activation of autophagy by unfolded proteins during endoplasmic reticulum stress Yang, Xiaochen; Srivastava, Renu; Howell, Stephen H. The Plant Journal, Vol. 85, Issue 1 https://doi.org/10.1111/tpj.13091	journal	December 2015
Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation Nukarinen, Ella; Nägele, Thomas; Pedrotti, Lorenzo Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep31697	journal	August 2016
ABI1 and PP2CA Phosphatases Are Negative Regulators of Snf1-Related Protein Kinase1 Signaling in Arabidopsis Rodrigues, Américo; Adamo, Mattia; Crozet, Pierre The Plant Cell, Vol. 25, Issue 10 https://doi.org/10.1105/tpc.113.114066	journal	October 2013
Leaf Senescence and Starvation-Induced Chlorosis Are Accelerated by the Disruption of an Arabidopsis Autophagy Gene Hanaoka, Hideki; Noda, Takeshi; Shirano, Yumiko Plant Physiology, Vol. 129, Issue 3 https://doi.org/10.1104/pp.011024	journal	July 2002
Novel links in the plant TOR kinase signaling network Xiong, Yan; Sheen, Jen Current Opinion in Plant Biology, Vol. 28 https://doi.org/10.1016/j.pbi.2015.09.006	journal	December 2015
Two SNF1-Related Protein Kinases from Spinach Leaf Phosphorylate and Inactivate 3-Hydroxy-3-Methylglutaryl-Coenzyme A Reductase, Nitrate Reductase, and Sucrose Phosphate Synthase in Vitro Sugden, Christopher; Donaghy, Paul G.; Halford, Nigel G. Plant Physiology, Vol. 120, Issue 1 https://doi.org/10.1104/pp.120.1.257	journal	May 1999
AMPK Phosphorylation of Raptor Mediates a Metabolic Checkpoint Gwinn, Dana M.; Shackelford, David B.; Egan, Daniel F. Molecular Cell, Vol. 30, Issue 2 https://doi.org/10.1016/j.molcel.2008.03.003	journal	April 2008
Antisense repression of StubGAL83 affects root and tuber development in potato Lovas, Agnes; Bimbo, Andrea; Szabo, Laszlo The Plant Journal, Vol. 33, Issue 1 https://doi.org/10.1046/j.1365-313X.2003.016015.x	journal	January 2003
Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene Menand, B.; Desnos, T.; Nussaume, L. Proceedings of the National Academy of Sciences, Vol. 99, Issue 9 https://doi.org/10.1073/pnas.092141899	journal	April 2002
Growth Arrest by Trehalose-6-Phosphate: An Astonishing Case of Primary Metabolite Control over Growth by Way of the SnRK1 Signaling Pathway Delatte, Thierry L.; Sedijani, Prapti; Kondou, Youichi Plant Physiology, Vol. 157, Issue 1 https://doi.org/10.1104/pp.111.180422	journal	July 2011
Bacterial Expression of the Catalytic Domain of 3-Hydroxy-3-Methylglutaryl-CoA Reductase (Isoform HMGR1) from Arabidopsis thaliana, and Its Inactivation by Phosphorylation at Ser577 by Brassica oleracea 3-Hydroxy-3-Methylglutaryl-CoA Reductase Kinase Dale, Susan; Arro, Montserrat; Becerra, Beatriz European Journal of Biochemistry, Vol. 233, Issue 2 https://doi.org/10.1111/j.1432-1033.1995.506_2.x	journal	October 1995
Isolation of autophagocytosis mutants of Saccharomyces cerevisiae Thumm, M.; Egner, R.; Koch, B. FEBS Letters, Vol. 349, Issue 2 https://doi.org/10.1016/0014-5793(94)00672-5	journal	August 1994
Antagonistic Controls of Autophagy and Glycogen Accumulation by Snf1p, the Yeast Homolog of AMP-Activated Protein Kinase, and the Cyclin-Dependent Kinase Pho85p Wang, Z.; Wilson, W. A.; Fujino, M. A. Molecular and Cellular Biology, Vol. 21, Issue 17 https://doi.org/10.1128/MCB.21.17.5742-5752.2001	journal	September 2001
Similar substrate recognition motifs for mammalian AMP-activated protein kinase, higher plant HMG-CoA reductase kinase-A, yeast SNF1, and mammalian calmodulin-dependent protein kinase I Dale, Susan; Wilson, Wayne A.; Edelman, Arthur M. FEBS Letters, Vol. 361, Issue 2-3 https://doi.org/10.1016/0014-5793(95)00172-6	journal	March 1995
Inhibition of SNF1-Related Protein Kinase1 Activity and Regulation of Metabolic Pathways by Trehalose-6-Phosphate Zhang, Yuhua; Primavesi, Lucia F.; Jhurreea, Deveraj Plant Physiology, Vol. 149, Issue 4 https://doi.org/10.1104/pp.108.133934	journal	February 2009
Regulation of macroautophagy by mTOR and Beclin 1 complexes Pattingre, Sophie; Espert, Lucile; Biard-Piechaczyk, Martine Biochimie, Vol. 90, Issue 2 https://doi.org/10.1016/j.biochi.2007.08.014	journal	February 2008
Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana Chen, Liang; Liao, Bin; Qi, Hua Autophagy, Vol. 11, Issue 12 https://doi.org/10.1080/15548627.2015.1112483	journal	December 2015
Degradation of Oxidized Proteins by Autophagy during Oxidative Stress in Arabidopsis Xiong, Yan; Contento, Anthony L.; Nguyen, Phan Quang Plant Physiology, Vol. 143, Issue 1 https://doi.org/10.1104/pp.106.092106	journal	November 2006
A central integrator of transcription networks in plant stress and energy signalling Baena-González, Elena; Rolland, Filip; Thevelein, Johan M. Nature, Vol. 448, Issue 7156 https://doi.org/10.1038/nature06069	journal	August 2007
Target of Rapamycin Regulates Development and Ribosomal RNA Expression through Kinase Domain in Arabidopsis Ren, Maozhi; Qiu, Shuqing; Venglat, Prakash Plant Physiology, Vol. 155, Issue 3 https://doi.org/10.1104/pp.110.169045	journal	January 2011
Autophagy: machinery and regulation Yin, Zhangyuan; Pascual, Clarence; Klionsky, Daniel Microbial Cell, Vol. 3, Issue 12 https://doi.org/10.15698/mic2016.12.546	journal	December 2016
The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function Broeckx, Tom; Hulsmans, Sander; Rolland, Filip Journal of Experimental Botany, Vol. 67, Issue 22 https://doi.org/10.1093/jxb/erw416	journal	November 2016
Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants Halford, Nigel G.; Hey, Sandra J. Biochemical Journal, Vol. 419, Issue 2 https://doi.org/10.1042/BJ20082408	journal	March 2009
Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes Li, Xiaojuan; Cai, Wenguo; Liu, Yanlin Proceedings of the National Academy of Sciences, Vol. 114, Issue 10 https://doi.org/10.1073/pnas.1618782114	journal	February 2017
TOR-Dependent and -Independent Pathways Regulate Autophagy in Arabidopsis thaliana Pu, Yunting; Luo, Xinjuan; Bassham, Diane C. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01204	journal	July 2017
The Trehalose 6-Phosphate/SnRK1 Signaling Pathway Primes Growth Recovery following Relief of Sink Limitation Nunes, C.; O'Hara, L. E.; Primavesi, L. F. PLANT PHYSIOLOGY, Vol. 162, Issue 3 https://doi.org/10.1104/pp.113.220657	journal	June 2013
Isoform-specific Subcellular Localization among 14-3-3 Proteins in Arabidopsis Seems to be Driven by Client Interactions Paul, Anna-Lisa; Sehnke, Paul C.; Ferl, Robert J. Molecular Biology of the Cell, Vol. 16, Issue 4 https://doi.org/10.1091/mbc.E04-09-0839	journal	April 2005
Autophagy Regulates Programmed Cell Death during the Plant Innate Immune Response Liu, Yule; Schiff, Michael; Czymmek, Kirk Cell, Vol. 121, Issue 4 https://doi.org/10.1016/j.cell.2005.03.007	journal	May 2005
LKB1 Is the Upstream Kinase in the AMP-Activated Protein Kinase Cascade Woods, Angela; Johnstone, Stephen R.; Dickerson, Kristina Current Biology, Vol. 13, Issue 22 https://doi.org/10.1016/j.cub.2003.10.031	journal	November 2003
SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants Mair, Andrea; Pedrotti, Lorenzo; Wurzinger, Bernhard eLife, Vol. 4 https://doi.org/10.7554/eLife.05828	journal	August 2015
Geminivirus AL2 and L2 Proteins Interact with and Inactivate SNF1 Kinase Hao, Linhui; Wang, Hui; Sunter, Garry The Plant Cell, Vol. 15, Issue 4 https://doi.org/10.1105/tpc.009530	journal	March 2003
Autophagy is required for tolerance of drought and salt stress in plants Liu, Yimo; Xiong, Yan; Bassham, Diane C. Autophagy, Vol. 5, Issue 7 https://doi.org/10.4161/auto.5.7.9290	journal	October 2009
Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein: Visualization of autophagy in Arabidopsis Contento, Anthony L.; Xiong, Yan; Bassham, Diane C. The Plant Journal, Vol. 42, Issue 4 https://doi.org/10.1111/j.1365-313X.2005.02396.x	journal	April 2005
The APG8/12-activating Enzyme APG7 Is Required for Proper Nutrient Recycling and Senescence in Arabidopsis thaliana Doelling, Jed H.; Walker, Joseph M.; Friedman, Eric M. Journal of Biological Chemistry, Vol. 277, Issue 36 https://doi.org/10.1074/jbc.M204630200	journal	June 2002
Raptor, a Binding Partner of Target of Rapamycin (TOR), Mediates TOR Action Hara, Kenta; Maruki, Yoshiko; Long, Xiaomeng Cell, Vol. 110, Issue 2 https://doi.org/10.1016/S0092-8674(02)00833-4	journal	July 2002

Similar Records

The UBA domain of SnRK1 promotes activation and maintains catalytic activity

Journal Article · Thu Feb 15 00:00:00 EST 2018 · Biochemical and Biophysical Research Communications · OSTI ID:1373990

Emanuelle, Shane

SIRT1 inactivation induces inflammation through the dysregulation of autophagy in human THP-1 cells

Journal Article · Fri Oct 12 00:00:00 EDT 2012 · Biochemical and Biophysical Research Communications · OSTI ID:1373990

Takeda-Watanabe, Ai; Kitada, Munehiro; Kanasaki, Keizo; +1 more

Trehalose 6-Phosphate Positively Regulates Fatty Acid Synthesis by Stabilizing WRINKLED1

Journal Article · Mon Sep 24 00:00:00 EDT 2018 · Plant Cell · OSTI ID:1373990

Zhai, Zhiyang; Keereetaweep, Jantana; Liu, Hui; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Autophagic cell death
Seedlings
Plant resistance to abiotic stress
Arabidopsis thaliana
Liquid chromatography-mass spectrometry
Osmotic shock
Regulator genes
Sucrose

Title: SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana

Citation Formats

References (72)

Similar Records

Related Subjects