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Plant SnRK1 Kinases: Structure, Regulation, and Function

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AMP-activated Protein Kinase

Part of the book series: Experientia Supplementum ((EXS,volume 107))

Abstract

SnRK1 is an evolutionarily conserved protein kinase complex that regulates energy homeostasis in plants. In doing so, it promotes tolerance to adverse environmental conditions and influences a large array of growth and developmental processes. SnRK1 shares clear structural and functional similarities with its orthologs, yeast SNF1 and mammalian AMPK, but has evolved unique features that presumably provide a better adaptation to an autotrophic lifestyle. In this chapter, we review current knowledge on SnRK1, an atypical member of the SNF1/AMPK family, providing insight into its structure, regulation, and functions.

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References

  • Alderson A, Sabelli PA, Dickinson JR, Cole D, Richardson M, Kreis M, Shewry PR, Halford NG (1991) Complementation of snf1, a mutation affecting global regulation of carbon metabolism in yeast, by a plant protein kinase cDNA. Proc Natl Acad Sci USA 88:8602–8605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ananieva EA, Gillaspy GE, Ely A, Burnette RN, Erickson FL (2008) Interaction of the WD40 domain of a myoinositol polyphosphate 5-phosphatase with SnRK1 links inositol, sugar, and stress signaling. Plant Physiol 148:1868–1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avila J, Gregory OG, Su D, Deeter TA, Chen S, Silva-Sanchez C, Xu S, Martin GB, Devarenne TP (2012) The β-subunit of the SnRK1 complex is phosphorylated by the plant cell death suppressor Adi3. Plant Physiol 159:1277–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avila-Castañeda A, Gutiérrez-Granados N, Ruiz-Gayosso A, Sosa-Peinado A, Martínez-Barajas E, Coello P (2014) Structural and functional basis for starch binding in the SnRK1 subunits AKINβ2 and AKINβγ. Front Plant Sci 5:199

    PubMed  PubMed Central  Google Scholar 

  • Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942

    Article  PubMed  CAS  Google Scholar 

  • Ball KL, Dale S, Weekes J, Hardie DG (1994) Biochemical characterization of two forms of 3-hydroxy-3-methylglutaryl-CoA reductase kinase from cauliflower (Brassica oleracia). Eur J Biochem 219:743–750

    Article  CAS  PubMed  Google Scholar 

  • Bateman A (1997) The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem Sci 22:12–13

    Article  CAS  PubMed  Google Scholar 

  • Beczner F, Dancs G, Sos-Hegedus A, Antal F, Banfalvi Z (2010) Interaction between SNF1-related kinases and a cytosolic pyruvate kinase of potato. J Plant Physiol 167:1046–1051

    Article  CAS  PubMed  Google Scholar 

  • Bhalerao RP, Salchert K, Bakó L, Okrész L, Szabados L, Muranaka T, Machida Y, Schell J, Koncz C (1999) Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc Natl Acad Sci U S A 96:5322–5327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bitrián M, Roodbarkelari F, Horváth M, Koncz C (2011) BAC-recombineering for studying plant gene regulation: developmental control and cellular localization of SnRK1 kinase subunits. Plant J 65:829–842

    Article  PubMed  CAS  Google Scholar 

  • Blasing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–3281

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bouly JP, Gissot L, Lessard P, Kreis M, Thomas M (1999) Arabidopsis thaliana proteins related to the yeast SIP and SNF4 interact with AKINalpha1, an SNF1-like protein kinase. Plant J 18:541–550

    Article  CAS  PubMed  Google Scholar 

  • Bradford KJ, Downie AB, Gee OH, Alvarado V, Yang H, Dahal P (2003) Abscisic acid and gibberellin differentially regulate expression of genes of the SNF1-related kinase complex in tomato seeds. Plant Physiol 132:1560–1576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin J-F, Wu S-H, Swidzinski J, Ishizaki K et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  CAS  PubMed  Google Scholar 

  • Buitink J, Thomas M, Gissot L, Leprince O (2003) Starvation, osmotic stress and desiccation tolerance lead to expression of different genes of the regulatory b and g subunits of the SnRK1 complex in germinating seeds of Medicago truncatula. Plant Cell Environ 27:55–67

    Article  Google Scholar 

  • Bustos DM, Iglesias AA (2003) Phosphorylated non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase from heterotrophic cells of wheat interacts with 14-3-3 proteins. Plant Physiol 133:2081–2088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carling D, Zammit VA, Hardie DG (1987) A common bicyclic protein kinase cascade inactivates the regulatory enzymes of fatty acid and cholesterol biosynthesis. FEBS Lett 223:217–222

    Article  CAS  PubMed  Google Scholar 

  • Carling D, Aguan K, Woods A, Verhoeven AJ, Beri RK, Brennan CH, Sidebottom C, Davison MD, Scott J (1994) Mammalian AMP-activated protein kinase is homologous to yeast and plant protein kinases involved in the regulation of carbon metabolism. J Biol Chem 269:11442–11448

    CAS  PubMed  Google Scholar 

  • Carling D, Thornton C, Woods A, Sanders MJ (2012) AMP-activated protein kinase: new regulation, new roles? Biochem J 445:11–27

    Article  CAS  PubMed  Google Scholar 

  • Castro PH, Verde N, Lourenco T, Magalhaes AP, Tavares RM, Bejarano ER, Azevedo H (2015) SIZ1-dependent post-translational modification by SUMO modulates sugar signaling and metabolism in Arabidopsis thaliana. Plant Cell Physiol 56(12):2297–2311

    Article  CAS  PubMed  Google Scholar 

  • Cernadas RA, Camillo LR, Benedetti CE (2008) Transcriptional analysis of the sweet orange interaction with the citrus canker pathogens Xanthomonas axonopodis pv. citri and Xanthomonas axonopodis pv. aurantifolii. Mol Plant Pathol 9:609–631

    Article  CAS  PubMed  Google Scholar 

  • Chandrashekarappa DG, McCartney RR, Schmidt MC (2013) Ligand binding to the AMP-activated protein kinase active site mediates protection of the activation loop from dephosphorylation. J Biol Chem 288:89–98

    Article  CAS  PubMed  Google Scholar 

  • Chantranupong L, Wolfson Rachel L, Sabatini David M (2015) Nutrient-sensing mechanisms across evolution. Cell 161:67–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiang C-P, Li C-H, Jou Y, Chen Y-C, Lin Y-C, Yang F-Y, Huang N-C, Yen HE (2013) Suppressor of K+ transport growth defect 1 (SKD1) interacts with RING-type ubiquitin ligase and sucrose non-fermenting 1-related protein kinase (SnRK1) in the halophyte ice plant. J Exp Bot 64:2385–2400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho Y-H, Hong J-W, Kim E-C, Yoo S-D (2012) Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol 158:1955–1964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choudhary MK, Nomura Y, Wang L, Nakagami H, Somers DE (2015) Quantitative circadian phosphoproteomic analysis of Arabidopsis reveals extensive clock control of key components in physiological, metabolic and signaling pathways. Mol Cell Proteomics 14:2243–2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coello P, Martínez-Barajas E (2014a) The activity of SnRK1 is increased in Phaseolus vulgaris seeds in response to a reduced nutrient supply. Front Plant Sci 5:196

    Article  PubMed  PubMed Central  Google Scholar 

  • Coello P, Martínez-Barajas E (2014b) SnRK1 is differentially regulated in the cotyledon and embryo axe of bean (Phaseolus vulgaris L) seeds. Plant Physiol Biochem 80:153–159

    Article  CAS  PubMed  Google Scholar 

  • Coello P, Hey SJ, Halford NG (2011) The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. J Exp Bot 62:883–893

    Article  CAS  PubMed  Google Scholar 

  • Coello P, Hirano E, Hey SJ, Muttucumaru N, Martinez-Barajas E, Parry MAJ, Halford NG (2012) Evidence that abscisic acid promotes degradation of SNF1-related protein kinase (SnRK) 1 in wheat and activation of a putative calcium-dependent SnRK2. J Exp Bot 63:913–924

    Article  CAS  PubMed  Google Scholar 

  • Confraria A, Martinho C, Elias A, Rubio-Somoza I, Baena-Gonzalez E (2013) miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis. Front Plant Sci 4:197

    Article  PubMed  PubMed Central  Google Scholar 

  • Contento AL, Kim S-J, Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol 135:2330–2347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crozet P, Jammes F, Valot B, Ambard-Bretteville F, Nessler S, Hodges M, Vidal J, Thomas M (2010) Cross-phosphorylation between Arabidopsis thaliana sucrose nonfermenting 1-related protein kinase 1 (AtSnRK1) and its activating kinase (AtSnAK) determines their catalytic activities. J Biol Chem 285:12071–12077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crozet P, Margalha L, Confraria A, Rodrigues A, Martinho C, Adamo M, Elias CA, Baena-González E (2014) Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases. Front Plant Sci 5:190

    Article  PubMed  PubMed Central  Google Scholar 

  • Crozet P, Margalha L, Butowt R, Fernandes N, Elias A, Orosa B, Tomanov K, Teige M, Bachmair A, Sadanandom A et al (2016) SUMOylation represses SnRK1 signaling in Arabidopsis. Plant J 85:120–133

    Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Dale S, Arro M, Becerra B, Morrice NG, Boronat A, Hardie DG, Ferrer A (1995a) 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. Eur J Biochem 233:506–513

    Article  CAS  PubMed  Google Scholar 

  • Dale S, Wilson WA, Edelman AM, Hardie DG (1995b) 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. FEBS Lett 361:191–195

    Article  CAS  PubMed  Google Scholar 

  • Davies SP, Hawley SA, Woods A, Carling D, Haystead TA, Hardie DG (1994) Purification of the AMP-activated protein kinase on ATP-gamma-sepharose and analysis of its subunit structure. Eur J Biochem 223:351–357

    Article  CAS  PubMed  Google Scholar 

  • De Block M, Van Lijsebettens M (2011) Energy efficiency and energy homeostasis as genetic and epigenetic components of plant performance and crop productivity. Curr Opin Plant Biol 14:275–282

    Article  PubMed  CAS  Google Scholar 

  • Debast S, Nunes-Nesi A, Hajirezaei MR, Hofmann J, Sonnewald U, Fernie AR, Börnke F (2011) Altering trehalose-6-phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol 156:1754–1771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas P, Pigaglio E, Ferrer A, Halford NG, MacKintosh C (1997) Three spinach leaf nitrate reductase-3-hydroxy-3-methylglutaryl-CoA reductase kinases that are regulated by reversible phosphorylation and/or Ca2+ ions. Biochem J 325(Pt 1):101–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elrouby N, Coupland G (2010) Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes. Proc Natl Acad Sci USA 107:17415–17420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emanuelle S, Hossain MI, Moller IE, Pedersen HL, van de Meene AML, Doblin MS, Koay A, Oakhill JS, Scott JW, Willats WGT et al (2015) SnRK1 from Arabidopsis thaliana is an atypical AMPK. Plant J 82:183–192

    Article  CAS  PubMed  Google Scholar 

  • Engelsberger WR, Schulze WX (2012) Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings. Plant J 69:978–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farrás R, Ferrando A, Jásik J, Kleinow T, Okrész L, Tiburcio A, Salchert K, del Pozo C, Schell J, Koncz C (2001) SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J 20:2742–2756

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrando A, Koncz-Kalman Z, Farras R, Tiburcio A, Schell J, Koncz C (2001) Detection of in vivo protein interactions between Snf1-related kinase subunits with intron-tagged epitope-labelling in plants cells. Nucleic Acids Res 29:3685–3693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fordham-Skelton AP, Chilley P, Lumbreras V, Reignoux S, Fenton TR, Dahm CC, Pages M, Gatehouse JA (2002) A novel higher plant protein tyrosine phosphatase interacts with SNF1-related protein kinases via a KIS (kinase interaction sequence) domain. Plant J 29:705–715

    Article  CAS  PubMed  Google Scholar 

  • Fragoso S, Espíndola L, Páez-Valencia J, Gamboa A, Camacho Y, Martínez-Barajas E, Coello P (2009) SnRK1 isoforms AKIN10 and AKIN11 are differentially regulated in Arabidopsis plants under phosphate starvation. Plant Physiol 149:1906–1916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghillebert R, Swinnen E, Wen J, Vandesteene L, Ramon M, Norga K, Rolland F, Winderickx J (2011) The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBS J 278:3978–3990

    Article  CAS  PubMed  Google Scholar 

  • Gissot L, Polge C, Bouly J-P, Lemaitre T, Kreis M, Thomas M (2004) AKINbeta3, a plant specific SnRK1 protein, is lacking domains present in yeast and mammals non-catalytic beta-subunits. Plant Mol Biol 56:747–759

    Article  CAS  PubMed  Google Scholar 

  • Gissot L, Polge C, Jossier M, Girin T, Bouly J-P, Kreis M, Thomas M (2006) AKINbetagamma contributes to SnRK1 heterotrimeric complexes and interacts with two proteins implicated in plant pathogen resistance through its KIS/GBD sequence. Plant Physiol 142:931–944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glinski M, Weckwerth W (2005) Differential multisite phosphorylation of the trehalose-6-phosphate synthase gene family in Arabidopsis thaliana: a mass spectrometry-based process for multiparallel peptide library phosphorylation analysis. Mol Cell Proteomics 4:1614–1625

    Article  CAS  PubMed  Google Scholar 

  • Gomez LD, Baud S, Gilday A, Li Y, Graham IA (2006) Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J 46:69–84

    Article  CAS  PubMed  Google Scholar 

  • Gowans GJ, Hawley SA, Ross FA, Hardie DG (2013) AMP is a true physiological regulator of AMP-activated protein kinase by both allosteric activation and enhancing net phosphorylation. Cell Metab 18:556–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guérinier T, Millan L, Crozet P, Oury C, Rey F, Valot B, Mathieu C, Vidal J, Hodges M, Thomas M et al (2013) Phosphorylation of p27(KIP) (1) homologs KRP6 and 7 by SNF1-related protein kinase-1 links plant energy homeostasis and cell proliferation. Plant J 75:515–525

    Article  PubMed  CAS  Google Scholar 

  • Halford NG, Hardie DG (1998) SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol Biol 37:735–748

    Article  CAS  PubMed  Google Scholar 

  • Halford NG, Hey SJ (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419:247–259

    Article  CAS  PubMed  Google Scholar 

  • Halford NG, Hey S, Jhurreea D, Laurie S, McKibbin RS, Paul M, Zhang Y (2003) Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J Exp Bot 54:467–475

    Article  CAS  PubMed  Google Scholar 

  • Hanks SK, Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9:576–596

    CAS  PubMed  Google Scholar 

  • Hao L, Wang H, Sunter G, Bisaro DM (2003) Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15:1034–1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774–785

    Article  CAS  PubMed  Google Scholar 

  • Hardie DG (2014) AMP-activated protein kinase: maintaining energy homeostasis at the cellular and whole-body levels. Annu Rev Nutr 34:31–55

    Article  CAS  PubMed  Google Scholar 

  • Harthill JE, Meek SEM, Morrice N, Peggie MW, Borch J, Wong BHC, Mackintosh C (2006) Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. Plant J 47:211–223

    Article  CAS  PubMed  Google Scholar 

  • Hartmann L, Pedrotti L, Weiste C, Fekete A, Schierstaedt J, Göttler J, Kempa S, Krischke M, Dietrich K, Mueller MJ et al (2015) Crosstalk between two bZIP signaling pathways orchestrates salt-induced metabolic reprogramming in Arabidopsis roots. Plant Cell 27:2244–2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heazlewood JL, Durek P, Hummel J, Selbig J, Weckwerth W, Walther D, Schulze WX (2008) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res 36:D1015–1021

    Article  CAS  PubMed  Google Scholar 

  • Hedbacker K, Carlson M (2006) Regulation of the nucleocytoplasmic distribution of Snf1-Gal83 protein kinase. Eukaryotic Cell 5:1950–1956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedbacker K, Carlson M (2008) SNF1/AMPK pathways in yeast. Front Biosci 13:2408–2420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedbacker K, Townley R, Carlson M (2004) Cyclic AMP-dependent protein kinase regulates the subcellular localization of Snf1-Sip1 protein kinase. Mol Cell Biol 24:1836–1843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hendriks IA, D’souza RCJ, Yang B, Verlaan-de Vries M, Mann M, Vertegaal ACO (2014) Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 53:1053–1066

    Google Scholar 

  • Henry C, Bledsoe SW, Griffiths CA, Kollman A, Paul MJ, Sakr S, Lagrimini LM (2015) Differential role for trehalose metabolism in salt-stressed maize. Plant Physiol 169:1072–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hey S, Mayerhofer H, Halford NG, Dickinson JR (2007) DNA sequences from Arabidopsis, which encode protein kinases and function as upstream regulators of Snf1 in yeast. J Biol Chem 282:10472–10479

    Article  CAS  PubMed  Google Scholar 

  • Hofmann K, Bucher P (1996) The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem Sci 21:172–173

    Article  CAS  PubMed  Google Scholar 

  • Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR et al (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeda Y, Koizumi N, Kusano T, Sano H (2000) Specific binding of a 14-3-3 protein to autophosphorylated WPK4, an SNF1-related wheat protein kinase, and to WPK4-phosphorylated nitrate reductase. J Biol Chem 275, 41528

    CAS  PubMed  Google Scholar 

  • Im JH, Cho Y-H, Kim G-D, Kang G-H, Hong J-W, Yoo S-D (2014) Inverse modulation of the energy sensor Snf1-related protein kinase 1 on hypoxia adaptation and salt stress tolerance in Arabidopsis thaliana. Plant Cell Environ 37:2303–2312

    CAS  PubMed  Google Scholar 

  • Jeong E-Y, Seo PJ, Woo JC, Park C-M (2015) AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis. BMC Plant Biol 15:110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jiang R, Carlson M (1997) The Snf1 protein kinase and its activating subunit, Snf4, interact with distinct domains of the Sip1/Sip2/Gal83 component in the kinase complex. Mol Cell Biol 17:2099–2106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jørgensen AD, Nøhr J, Kastrup JS, Gajhede M, Sigurskjold BW, Sauer J, Svergun DI, Svensson B, Vestergaard B (2008) Small angle X-ray studies reveal that Aspergillus niger glucoamylase has a defined extended conformation and can form dimers in solution. J Biol Chem 283:14772–14780

    Article  PubMed  CAS  Google Scholar 

  • Jossier M, Bouly J-P, Meimoun P, Arjmand A, Lessard P, Hawley S, Grahame Hardie D, Thomas M (2009) SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J 59:316–328

    Article  CAS  PubMed  Google Scholar 

  • Kazgan N, Williams T, Forsberg LJ, Brenman JE (2010) Identification of a nuclear export signal in the catalytic subunit of AMP-activated protein kinase. Mol Biol Cell 21:3433–3442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerk D, Conley TR, Rodriguez FA, Tran HT, Nimick M, Muench DG, Moorhead GBG (2006) A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. Plant J 46:400–413

    Article  CAS  PubMed  Google Scholar 

  • Kim D-Y, Scalf M, Smith LM, Vierstra RD (2013) Advanced proteomic analyses yield a deep catalog of ubiquitylation targets in Arabidopsis. Plant Cell 25:1523–1540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleinow T, Bhalerao R, Breuer F, Umeda M, Salchert K, Koncz C (2000) Functional identification of an Arabidopsis snf4 ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast. Plant J 23:115–122

    Article  CAS  PubMed  Google Scholar 

  • Kleinow T, Himberta S, Krenza B, Jeskea H, Koncz C (2009) NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis. Plant Sci 177:360–370

    Article  CAS  Google Scholar 

  • Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci U S A 102:11118–11123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, Steup M et al (2009) STARCH-EXCESS4 is a laforin-like Phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21:334–346

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kulma A, Villadsen D, Campbell DG, Meek SEM, Harthill JE, Nielsen TH, Mackintosh C (2004) Phosphorylation and 14-3-3 binding of Arabidopsis 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase. Plant J 37:654–667

    Article  CAS  PubMed  Google Scholar 

  • Lane N, Martin W (2010) The energetics of genome complexity. Nature 467:929–934

    Article  CAS  PubMed  Google Scholar 

  • Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807

    Article  CAS  PubMed  Google Scholar 

  • Laurie S, McKibbin RS, Halford NG (2003) Antisense SNF1-related (SnRK1) protein kinase gene represses transient activity of an alpha-amylase (alpha-Amy2) gene promoter in cultured wheat embryos. J Exp Bot 54:739–747

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Terzaghi W, Gusmaroli G, Charron JB, Yoon HJ, Chen H, He YJ, Xiong Y, Deng XW (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20:152–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee K-W, Chen P-W, Lu C-A, Chen S, Yu S-M, Ho T-HD (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61

    PubMed  Google Scholar 

  • Li X-F, Li Y-J, An Y-H, Xiong L-J, Shao X-H, Wang Y, Sun Y (2009) AKINbeta1 is involved in the regulation of nitrogen metabolism and sugar signaling in Arabidopsis. J Integr Plant Biol 51:513–520

    Article  CAS  PubMed  Google Scholar 

  • Liang J, Shao SH, Xu Z-X, Hennessy B, Ding Z, Larrea M, Kondo S, Dumont DJ, Gutterman JU, Walker CL et al (2007) The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 9:218–224

    Article  CAS  PubMed  Google Scholar 

  • Lin J-F, Wu S-H (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628

    Article  CAS  PubMed  Google Scholar 

  • Lin C-R, Lee K-W, Chen C-Y, Hong Y-F, Chen J-L, Lu C-A, Chen K-T, Ho T-HD YS-M (2014) SnRK1A-interacting negative regulators modulate the nutrient starvation signaling sensor SnRK1 in source-sink communication in cereal seedlings under abiotic stress. Plant Cell 26:808–827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Chung HY, Lacatus G, Baliji S, Ruan J, Sunter G (2014) Altered expression of Arabidopsis genes in response to a multifunctional geminivirus pathogenicity protein. BMC Plant Biol 14:302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • López-Paz C, Vilela B, Riera M, Pagès M, Lumbreras V (2009) Maize AKINbetagamma dimerizes through the KIS/CBM domain and assembles into SnRK1 complexes. FEBS Lett 583:1887–1894

    Article  PubMed  CAS  Google Scholar 

  • Lovas A, Bimbó A, Szabó L, Bánfalvi Z (2003) Antisense repression of StubGAL83 affects root and tuber development in potato. Plant J 33:139–147

    Article  CAS  PubMed  Google Scholar 

  • Lu Z, Hunter T (2009) Degradation of activated protein kinases by ubiquitination. Annu Rev Biochem 78:435–475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu C-A, Lin C-C, Lee K-W, Chen J-L, Huang L-F, Ho S-L, Liu H-J, Hsing Y-I, Yu S-M (2007) The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19:2484–2499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lumbreras V, Alba MM, Kleinow T, Koncz C, Pagès M (2001) Domain fusion between SNF1-related kinase subunits during plant evolution. EMBO Rep 2:55–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Hanssen M, Lundgren K, Hernández L, Delatte T, Ehlert A, Liu C-M, Schluepmann H, Dröge-Laser W, Moritz T et al (2011) The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism. New Phytol 191:733–745

    Article  CAS  PubMed  Google Scholar 

  • Mackintosh RW, Davies SP, Clarke PR, Weekes J, Gillespie JG, Gibb BJ, Hardie DG (1992) Evidence for a protein kinase cascade in higher plants. 3-Hydroxy-3-methylglutaryl-CoA reductase kinase. Eur J Biochem 209:923–931

    Article  CAS  PubMed  Google Scholar 

  • Mair A, Pedrotti L, Wurzinger B, Anrather D, Simeunovic A, Weiste C, Valerio C, Dietrich K, Kirchler T, Nägele T et al (2015) SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants. eLife 4

    Google Scholar 

  • Maor R, Jones A, Nühse TS, Studholme DJ, Peck SC, Shirasu K (2007) Multidimensional protein identification technology (MudPIT) analysis of ubiquitinated proteins in plants. Mol Cell Proteomics 6:601–610

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Barajas E, Delatte T, Schluepmann H, de Jong GJ, Somsen GW, Nunes C, Primavesi LF, Coello P, Mitchell RAC, Paul MJ (2011) Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity. Plant Physiol 156:373–381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matiolli CC, Tomaz JP, Duarte GT, Prado FM, Del Bem LEV, Silveira AB, Gauer L, Corrêa LGG, Drumond RD, Viana AJC et al (2011) The Arabidopsis bZIP gene AtbZIP63 is a sensitive integrator of transient ABA and glucose signals. Plant Physiol 157:692–705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McBride A, Ghilagaber S, Nikolaev A, Hardie DG (2009) The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor. Cell Metab 9:23–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCartney RR, Schmidt MC (2001) Regulation of Snf1 kinase. Activation requires phosphorylation of threonine 210 by an upstream kinase as well as a distinct step mediated by the Snf4 subunit. J Biol Chem 276:36460–36466

    Article  CAS  PubMed  Google Scholar 

  • Mccormick AJ, Kruger NJ (2015) Lack of fructose 2,6-bisphosphate compromises photosynthesis and growth in Arabidopsis in fluctuating environments. Plant J 81:670–683

    Article  CAS  PubMed  Google Scholar 

  • McMichael RW, Bachmann M, Huber SC (1995) Spinach leaf sucrose-phosphate synthase and nitrate reductase are phosphorylated/inactivated by multiple protein kinases in vitro. Plant Physiol 108:1077–1082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchelhill KI, Stapleton D, Gao G, House C, Michell B, Katsis F, Witters LA, Kemp BE (1994) Mammalian AMP-activated protein kinase shares structural and functional homology with the catalytic domain of yeast Snf1 protein kinase. J Biol Chem 269:2361–2364

    CAS  PubMed  Google Scholar 

  • Moorhead G, Douglas P, Morrice N, Scarabel M, Aitken A, MacKintosh C (1996) Phosphorylated nitrate reductase from spinach leaves is inhibited by 14-3-3 proteins and activated by fusicoccin. Curr Biol 6:1104–1113

    Article  CAS  PubMed  Google Scholar 

  • Muranaka T, Banno H, Machida Y (1994) Characterization of tobacco protein kinase NPK5, a homolog of Saccharomyces cerevisiae SNF1 that constitutively activates expression of the glucose-repressible SUC2 gene for a secreted invertase of S. cerevisiae. Mol Cell Biol 14:2958–2965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K (2010) Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 153:1161–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nayak V, Zhao K, Wyce A, Schwartz MF, Lo W-S, Berger SL, Marmorstein R (2006) Structure and dimerization of the kinase domain from yeast Snf1, a member of the Snf1/AMPK protein family. Structure 14:477–485

    Article  CAS  PubMed  Google Scholar 

  • Nietzsche M, Schießl I, Börnke F (2014) The complex becomes more complex: protein-protein interactions of SnRK1 with DUF581 family proteins provide a framework for cell- and stimulus type-specific SnRK1 signaling in plants. Front Plant Sci 5:54

    Article  PubMed  PubMed Central  Google Scholar 

  • Niittylä T, Comparot-Moss S, Lue W-L, Messerli G, Trevisan M, Seymour MDJ, Gatehouse JA, Villadsen D, Smith SM, Chen J et al (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J Biol Chem 281:11815–11818

    Article  PubMed  CAS  Google Scholar 

  • Nunes C, O’Hara LE, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, Paul MJ (2013a) The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162:1720–1732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Sagar R, Fevereiro PS, Davis BG, Paul MJ (2013b) Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol Biochem 63:89–98

    Article  CAS  PubMed  Google Scholar 

  • O’Brien M, Kaplan-Levy RN, Quon T, Sappl PG, Smyth DR (2015) PETAL LOSS, a trihelix transcription factor that represses growth in Arabidopsis thaliana, binds the energy-sensing SnRK1 kinase AKIN10. J Exp Bot 66:2475–2485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oakhill JS, Chen Z-P, Scott JW, Steel R, Castelli LA, Ling N, Macaulay SL, Kemp BE (2010) β-Subunit myristoylation is the gatekeeper for initiating metabolic stress sensing by AMP-activated protein kinase (AMPK). Proc Natl Acad Sci USA 107:19237–19241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oakhill JS, Steel R, Chen Z-P, Scott JW, Ling N, Tam S, Kemp BE (2011) AMPK is a direct adenylate charge-regulated protein kinase. Science 332:1433–1435

    Article  CAS  PubMed  Google Scholar 

  • Oakhill JS, Scott JW, Kemp BE (2012) AMPK functions as an adenylate charge-regulated protein kinase. Trends Endocrinol Metab 23:125–132

    Article  CAS  PubMed  Google Scholar 

  • Osuna D, Usadel B, Morcuende R, Gibon Y, Blasing OE, Hohne M, Gunter M, Kamlage B, Trethewey R, Scheible WR et al (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49:463–491

    Article  CAS  PubMed  Google Scholar 

  • Palenchar PM, Kouranov A, Lejay LV, Coruzzi GM (2004) Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol 5:R91

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul M (2007) Trehalose 6-phosphate. Curr Opin Plant Biol 10:303–309

    Article  CAS  PubMed  Google Scholar 

  • Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441

    Article  CAS  PubMed  Google Scholar 

  • Pellicena P, Kuriyan J (2006) Protein-protein interactions in the allosteric regulation of protein kinases. Curr Opin Struct Biol 16:702–709

    Article  CAS  PubMed  Google Scholar 

  • Piattoni CV, Bustos DM, Guerrero SA, Iglesias AA (2011) Nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase is phosphorylated in wheat endosperm at serine-404 by an SNF1-related protein kinase allosterically inhibited by ribose-5-phosphate. Plant Physiol 156:1337–1350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pien S, Wyrzykowska J, Fleming AJ (2001) Novel marker genes for early leaf development indicate spatial regulation of carbohydrate metabolism within the apical meristem. Plant J 25:663–674

    Article  CAS  PubMed  Google Scholar 

  • Pierre M, Traverso JA, Boisson B, Domenichini S, Bouchez D, Giglione C, Meinnel T (2007) N-Myristoylation regulates the SnRK1 pathway in Arabidopsis. Plant Cell 19:2804–2821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polekhina G, Gupta A, Michell BJ, Van Denderen B, Murthy S, Feil SC, Jennings IG, Campbell DJ, Witters LA, Parker MW et al (2003) AMPK beta subunit targets metabolic stress sensing to glycogen. Curr Biol 13:867–871

    Article  CAS  PubMed  Google Scholar 

  • Polekhina G, Gupta A, Van Denderen BJW, Feil SC, Kemp BE, Stapleton D, Parker MW (2005) Structural basis for glycogen recognition by AMP-activated protein kinase. Structure 13:1453–1462

    Article  CAS  PubMed  Google Scholar 

  • Polge C, Thomas M (2007) SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci 12:20–28

    Article  CAS  PubMed  Google Scholar 

  • Polge C, Jossier M, Crozet P, Gissot L, Thomas M (2008) Beta-subunits of the SnRK1 complexes share a common ancestral function together with expression and function specificities; physical interaction with nitrate reductase specifically occurs via AKINbeta1-subunit. Plant Physiol 148:1570–1582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price J, Laxmi A, St Martin SK, Jang J-C (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purcell P, Smith AM, Halford NG (1998) Antisense expression of sucrose non-fermenting-1-related protein kinase sequence in potato results in decreased expression of sucrose synthase in tubers and loss of sucrose-inducibility of sucrose synthase transcripts in leaves. Plant J 14:195–203

    Article  CAS  Google Scholar 

  • Radchuk R, Radchuk V, Weschke W, Borisjuk L, Weber H (2006) Repressing the expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiol 140:263–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radchuk R, Emery RJN, Weier D, Vigeolas H, Geigenberger P, Lunn JE, Feil R, Weschke W, Weber H (2010) Sucrose non-fermenting kinase 1 (SnRK1) coordinates metabolic and hormonal signals during pea cotyledon growth and differentiation. Plant J 61:324–338

    Article  CAS  PubMed  Google Scholar 

  • Ramon M, De Smet I, Vandesteene L, Naudts M, Leyman B, Van Dijck P, Rolland F, Beeckman T, Thevelein JM (2009) Extensive expression regulation and lack of heterologous enzymatic activity of the class II trehalose metabolism proteins from Arabidopsis thaliana. Plant Cell Environ 32:1015–1032

    Article  CAS  PubMed  Google Scholar 

  • Ramon M, Ruelens P, Li Y, Sheen J, Geuten K, Rolland F (2013) The hybrid four-CBS-domain KINβγ subunit functions as the canonical γ subunit of the plant energy sensor SnRK1. Plant J 75:11–25

    Article  CAS  PubMed  Google Scholar 

  • Riek U, Scholz R, Konarev P, Rufer A, Suter M, Nazabal A, Ringler P, Chami M, Müller SA, Neumann D et al (2008) Structural properties of AMP-activated protein kinase: dimerization, molecular shape, and changes upon ligand binding. J Biol Chem 283:18331–18343

    Article  CAS  PubMed  Google Scholar 

  • Robaglia C, Thomas M, Meyer C (2012) Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 15:301–307

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues A, Adamo M, Crozet P, Margalha L, Confraria A, Martinho C, Elias A, Rabissi A, Lumbreras V, González-Guzmán M et al (2013) ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell 25:3871–3884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Rook F, Gerrits N, Kortstee A, van Kampen M, Borrias M, Weisbeek P, Smeekens S (1998) Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J 15:253–263

    Article  CAS  PubMed  Google Scholar 

  • Rosnoblet C, Aubry C, Leprince O, Vu BL, Rogniaux H, Buitink J (2007) The regulatory gamma subunit SNF4b of the sucrose non-fermenting-related kinase complex is involved in longevity and stachyose accumulation during maturation of Medicago truncatula seeds. Plant J 51:47–59

    Article  CAS  PubMed  Google Scholar 

  • Rubio T, Vernia S, Sanz P (2013) Sumoylation of AMPKβ2 subunit enhances AMP-activated protein kinase activity. Mol Biol Cell 24:1801–1811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudolph MJ, Amodeo GA, Bai Y, Tong L (2005) Crystal structure of the protein kinase domain of yeast AMP-activated protein kinase Snf1. Biochem Biophys Res Commun 337:1224–1228

    Article  CAS  PubMed  Google Scholar 

  • Schluepmann H, Paul M (2009) Trehalose metabolites in Arabidopsis-elusive, active and central. Arabidopsis Book 7, e0122

    Article  PubMed  PubMed Central  Google Scholar 

  • Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci U S A 100:6849–6854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schluepmann H, van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S (2004) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol 135:879–890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholz R, Suter M, Weimann T, Polge C, Konarev PV, Thali RF, Tuerk RD, Viollet B, Wallimann T, Schlattner U et al (2009) Homo-oligomerization and activation of AMP-activated protein kinase are mediated by the kinase domain alphaG-helix. J Biol Chem 284:27425–27437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuck S, Camehl I, Gilardoni PA, Oelmueller R, Baldwin IT, Bonaventure G (2012) HSPRO controls early Nicotiana attenuata seedling growth during interaction with the fungus Piriformospora indica. Plant Physiol 160:929–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuck S, Baldwin IT, Bonaventure G (2013) HSPRO acts via SnRK1-mediated signaling in the regulation of Nicotiana attenuata seedling growth promoted by Piriformospora indica. Plant Signal Behav 8, e23537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci U S A 103:12935–12940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott JW, Hawley SA, Green KA, Anis M, Stewart G, Scullion GA, Norman DG, Hardie DG (2004) CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest 113:274–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen W, Hanley-Bowdoin L (2006) Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1- and mammalian AMPK-activating kinases. Plant Physiol 142:1642–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen W, Reyes MI, Hanley-Bowdoin L (2009) Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop. Plant Physiol 150:996–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Q, Liu Z, Song F, Xie Q, Hanley-Bowdoin L, Zhou X (2011) Tomato SlSnRK1 protein interacts with and phosphorylates betaC1, a pathogenesis protein encoded by a geminivirus beta-satellite. Plant Physiol 157:1394–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Q, Bao M, Zhou X (2012) A plant kinase plays roles in defense response against geminivirus by phosphorylation of a viral pathogenesis protein. Plant Signal Behav 7:888–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen W, Dallas MB, Goshe MB, Hanley-Bowdoin L (2014) SnRK1 phosphorylation of AL2 delays cabbage leaf curl virus infection in Arabidopsis. J Virol 88:10598–10612

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Short JD, Houston KD, Dere R, Cai S-L, Kim J, Johnson CL, Broaddus RR, Shen J, Miyamoto S, Tamanoi F et al (2008) AMP-activated protein kinase signaling results in cytoplasmic sequestration of p27. Cancer Res 68:6496–6506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Short JD, Dere R, Houston KD, Cai S-L, Kim J, Bergeron JM, Shen J, Liang J, Bedford MT, Mills GB et al (2010) AMPK-mediated phosphorylation of murine p27 at T197 promotes binding of 14-3-3 proteins and increases p27 stability. Mol Carcinog 49:429–439

    CAS  PubMed  Google Scholar 

  • Simpson-Lavy KJ, Johnston M (2013) SUMOylation regulates the SNF1 protein kinase. Proc Natl Acad Sci U S A 110:17432–17437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson-Lavy KJ, Bronstein A, Kupiec M, Johnston M (2015) Cross-talk between carbon metabolism and the DNA damage response in S. cerevisiae. Cell Rep 12:1865–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slocombe SP, Beaudoin F, Donaghy PG, Hardie DG, Dickinson JR, Halford NG (2004) SNF1-related protein kinase (snRK1) phosphorylates class I heat shock protein. Plant Physiol Biochem 42:111–116

    Article  CAS  PubMed  Google Scholar 

  • Stein SC, Woods A, Jones NA, Davison MD, Carling D (2000) The regulation of AMP-activated protein kinase by phosphorylation. Biochem J 345:437–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinberg GR, Kemp BE (2009) AMPK in health and disease. Physiol Rev 89:1025–1078

    Article  CAS  PubMed  Google Scholar 

  • Stitt M (1987) Fructose 2,6-bisphosphate and plant carbohydrate metabolism. Plant Physiol 84:201–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugden C, Crawford RM, Halford NG, Hardie DG (1999a) 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. Plant J 19:433–439

    Article  CAS  PubMed  Google Scholar 

  • Sugden C, Donaghy PG, Halford NG, Hardie DG (1999b) 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. Plant Physiol 120:257–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki A, Okamoto S, Lee S, Saito K, Shiuchi T, Minokoshi Y (2007) Leptin stimulates fatty acid oxidation and peroxisome proliferator-activated receptor alpha gene expression in mouse C2C12 myoblasts by changing the subcellular localization of the alpha2 form of AMP-activated protein kinase. Mol Cell Biol 27:4317–4327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szal B, Podgorska A (2012) The role of mitochondria in leaf nitrogen metabolism. Plant Cell Environ 35:1756–1768

    Article  CAS  PubMed  Google Scholar 

  • Szczesny R, Büttner D, Escolar L, Schulze S, Seiferth A, Bonas U (2010) Suppression of the AvrBs1-specific hypersensitive response by the YopJ effector homolog AvrBsT from Xanthomonas depends on a SNF1-related kinase. New Phytol 187:1058–1074

    Article  CAS  PubMed  Google Scholar 

  • Thelander M, Olsson T, Ronne H (2004) Snf1-related protein kinase 1 is needed for growth in a normal day–night light cycle. EMBO J 23:1900–1910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Tiessen A, Prescha K, Branscheid A, Palacios N, Mckibbin R, Halford NG, Geigenberger P (2003) Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. Plant J 35:490–500

    Article  CAS  PubMed  Google Scholar 

  • Toroser D, Plaut Z, Huber SC (2000) Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate. Plant Physiol 123:403–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traverso JA, Meinnel T, Giglione C (2008) Expanded impact of protein N-myristoylation in plants. Plant Signal Behav 3:501–502

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsai AY-L, Gazzarrini S (2012) AKIN10 and FUSCA3 interact to control lateral organ development and phase transitions in Arabidopsis. Plant J 69:809–821

    Article  CAS  PubMed  Google Scholar 

  • Tsai AY, Gazzarrini S (2014) Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture. Front Plant Sci 5:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsugama D, Liu S, Takano T (2012) A putative myristoylated 2C-type protein phosphatase, PP2C74, interacts with SnRK1 in Arabidopsis. FEBS Lett 586:693–698

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Sugiyama N, Takahashi F, Anderson JC, Ishihama Y, Peck SC, Shinozaki K (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci Signal 6:rs8

    Article  PubMed  CAS  Google Scholar 

  • Viana R, Towler MC, Pan DA, Carling D, Viollet B, Hardie DG, Sanz P (2007) A conserved sequence immediately N-terminal to the Bateman domains in AMP-activated protein kinase gamma subunits is required for the interaction with the beta subunits. J Biol Chem 282:16117–16125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Hao L, Shung CY, Sunter G, Bisaro DM (2003) Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15:3020–3032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Peng F, Li M, Yang L, Li G (2012) Expression of a heterologous SnRK1 in tomato increases carbon assimilation, nitrogen uptake and modifies fruit development. J Plant Physiol 169:1173–1182

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Xue L, Batelli G, Lee S, Hou Y-J, Van Oosten MJ, Zhang H, Tao WA, Zhu J-K (2013) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci U S A 110:11205–11210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warden SM, Richardson C, O’Donnell J, Stapleton D, Kemp BE, Witters LA (2001) Post-translational modifications of the beta-1 subunit of AMP-activated protein kinase affect enzyme activity and cellular localization. Biochem J 354:275–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weltmeier F, Rahmani F, Ehlert A, Dietrich K, Schutze K, Wang X, Chaban C, Hanson J, Teige M, Harter K et al (2009) Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development. Plant Mol Biol 69:107–119

    Article  CAS  PubMed  Google Scholar 

  • Wiatrowski HA, Van Denderen BJW, Berkey CD, Kemp BE, Stapleton D, Carlson M (2004) Mutations in the gal83 glycogen-binding domain activate the snf1/gal83 kinase pathway by a glycogen-independent mechanism. Mol Cell Biol 24:352–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiese A, Elzinga N, Wobbes B, Smeekens S (2005) Sucrose-induced translational repression of plant bZIP-type transcription factors. Biochem Soc Trans 33:272–275

    Article  CAS  PubMed  Google Scholar 

  • Williams T, Brenman JE (2008) LKB1 and AMPK in cell polarity and division. Trends Cell Biol 18:193–198

    Article  CAS  PubMed  Google Scholar 

  • Williams SP, Rangarajan P, Donahue JL, Hess JE, Gillaspy GE (2014) Regulation of sucrose non-fermenting related kinase 1 genes in Arabidopsis thaliana. Front Plant Sci 5:324

    PubMed  PubMed Central  Google Scholar 

  • Xiao B, Sanders MJ, Underwood E, Heath R, Mayer FV, Carmena D, Jing C, Walker PA, Eccleston JF, Haire LF et al (2011) Structure of mammalian AMPK and its regulation by ADP. Nature 472:230–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao Q, Bollinger C, Gao J, Xu D, Thelen JJ (2012) P(3)DB: an integrated database for plant protein phosphorylation. Front Plant Sci 3:206

    PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Shewry PR, Jones H, Barcelo P, Lazzeri PA, Halford NG (2001) Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J 28:431–441

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149:1860–1871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Deng Y, Song X, Miao M (2015) Trehalose-6-phosphate and SNF1-related protein kinase 1 are involved in the first-fruit inhibition of cucumber. J Plant Physiol 177:110–120

    Article  CAS  PubMed  Google Scholar 

  • Zourelidou M, de Torres-Zabala M, Smith C, Bevan MW (2002) Storekeeper defines a new class of plant-specific DNA-binding proteins and is a putative regulator of patatin expression. Plant J 30:489–497

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Pierre Crozet and Ana Confraria for criticism and suggestions on the manuscript and Nuno Margalha for valuable help with the figures. This work was supported by Fundação para a Ciência e a Tecnologia projects PTDC/BIA-PLA/3937/2012 and UID/Multi/04551/2013.

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Authors and Affiliations

  1. Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156, Oeiras, Portugal

    Leonor Margalha, Concetta Valerio & Elena Baena-González

Authors
  1. Leonor Margalha
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  2. Concetta Valerio
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  3. Elena Baena-González
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Corresponding author

Correspondence to Elena Baena-González .

Editor information

Editors and Affiliations

  1. Oral Medicine Department, Universidad de Sevilla, Sevilla, Spain

    Mario D. Cordero

  2. INSERM U1016 Institut Cochin CNRS UMR 8104, Université Paris Descartes, Paris, France

    Benoit Viollet

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© 2016 Springer International Publishing Switzerland

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Margalha, L., Valerio, C., Baena-González, E. (2016). Plant SnRK1 Kinases: Structure, Regulation, and Function. In: Cordero, M., Viollet, B. (eds) AMP-activated Protein Kinase. Experientia Supplementum, vol 107. Springer, Cham. https://doi.org/10.1007/978-3-319-43589-3_17

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