Skip to main content

Advertisement

SpringerLink
Log in

Master regulators in plant glucose signaling networks

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

The daily life of photosynthetic plants revolves around sugar production, transport, storage and utilization, and the complex sugar metabolic and signaling networks integrate internal regulators and environmental cues to govern and sustain plant growth and survival. Although diverse sugar signals have emerged as pivotal regulators from embryogenesis to senescence, glucose is the most ancient and conserved regulatory signal that controls gene and protein expression, cell-cycle progression, central and secondary metabolism, as well as growth and developmental programs. Glucose signals are perceived and transduced by two principal mechanisms: direct sensing through glucose sensors and indirect sensing via a variety of energy and metabolite sensors. This review focuses on the comparative and functional analyses of three glucose-modulated master regulators in Arabidopsis thaliana, the hexokinase1 (HXK1) glucose sensor, the energy sensor kinases KIN10/KIN11 inactivated by glucose, and the glucoseactivated target of rapamycin (TOR) kinase. These regulators are evolutionarily conserved, but have evolved universal and unique regulatory wiring and functions in plants and animals. They form protein complexes with multiple partners as regulators or effectors to serve distinct functions in different subcellular locales and organs, and play integrative and complementary roles from cellular signaling and metabolism to development in the plant glucose signaling networks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahn CS, Han JA, Lee HS, Lee S, Pai HS (2011) The PP2A regulatory subunit Tap46, a component of the TOR signaling pathway, modulates growth and metabolism in plants. Plant Cell 23:185–209

    CAS  PubMed Central  PubMed  Google Scholar 

  • Alonso R, Oñate-Sánchez L, Weltmeier F, Ehlert A, Diaz I, Dietrich K, Vicente-Carbajosa J, Dröge-Laser W (2009) A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell 21:1747–1761

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anderson GH, Veit B, Hanson MR (2005) The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol 3:12

    PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Avonce N, Leyman B, Mascorro-Gallardo JO, van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose 6-phosphtae synthase AtTPS1 gene is a regulator of glucose, abscisic acid and stress signalling. Plant Physiol 136:3649–3659

    CAS  PubMed Central  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–481

    PubMed Central  PubMed  Google Scholar 

  • Balasubramanian R, Karve A, Kandasamy M, Meagher RB, Moore B (2007) A role of F-actin in hexokinase-mediated glucose signaling. Plant Physiol 145:1423–1434.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bhalerao RP, Salchert K, Bako L, Okresz 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 USA 96:5322–5327

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  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

    PubMed Central  PubMed  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidainski J, Ishizaki K, Leaver CJ (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

    CAS  PubMed  Google Scholar 

  • Caldana C, Li Y, Leisse A, Zhang Y, Bartholomaeus L, Fernie AR, Willmitzer L, Giavalisco P (2013) Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant J 73:897–909

    CAS  PubMed  Google Scholar 

  • Celenza JL, Carlson M (1986) A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science 233:1175–1180.

    CAS  PubMed  Google Scholar 

  • Chary SN, Hicks GR, Choi YG, Carter D, Raikhel NV (2008) Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis. Plant Physiol 146:97–107

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cho YH, Yoo SD, Sheen J (2006) Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127:579–589

    CAS  PubMed  Google Scholar 

  • Cho JI, Ryoo N, Eom JS, Lee DW, Kim HB, Jeong SW, Lee YH, Kwon YK, Cho MH, Bhoo SH, Hahn TR, Park YI, Hwang I, Sheen J, Jeon JS (2009) Role of the rice hexokinases OsHXK5 and OsHXK6 as glucose sensors. Plant Physiol 149:745–759

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cho YH, Sheen J, Yoo SD (2010) Low glucose uncouples HXK1-dependent sugar signaling from stress and defense hormone ABA and C2H4 responses in Arabidopsis. Plant Physiol 152:1180–1182

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cho YH, Yoo SD (2011) Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLOS Genet 7:e1001263

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cho YH, Hong JW, Kim EC, Yoo SD (2012) Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol 158:1955–1964

    CAS  PubMed Central  PubMed  Google Scholar 

  • Claeyssen E, Rivoal J (2007) Isozymes of plant hexokinase: occurrence, properties and functions. Phytochem 68:709–731

    CAS  Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cornu M, Albert V, Hall MN (2013) mTOR in aging, metabolism, and cancer. Curr Opin Genet Dev 23:53–62

    CAS  PubMed  Google Scholar 

  • Danial NN, Gramm CF, Scorrano L, Zhang CY, Krauss S, Ranger AM, Data SR, Greenberg ME, Licklider LJ, Lowell BB, Gigi SP, Korsmeyer SJ (2003) BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424:952–956

    CAS  PubMed  Google Scholar 

  • De Jager SM, Scofield S, Huntley RP, Robinson AS, den Boer BG, Murray JA (2009) Dissecting regulatory pathways of G1/S control in Arabidopsis: common and distinct targets of CYCD3;1, E2Fa and E2Fc. Plant Mol Biol 71:345–365

    PubMed  Google Scholar 

  • De Jong F, Thodey K, Lejay LV, Bevan MW (2014) Glucose elevates NITRATE TRANSPORTER2.1 protein levels and nitrate transport activity independently of its HEXOKINASE1-mediated stimulation of NITRATE TRANSPORTER 2.1 expression. Plant Phyiol 164:308–320

    Google Scholar 

  • Delatte TL, Sedijani P, Kondou Y, Matsui M, de Jong GJ, Somsen GW, Wiese-Klinkenberg A, Primavesi LF, Paul MJ, Schluepmann H (2011) Growth arrest by trehalose-6-phosphate: an astonishing case of primary metabolite control over growth by way of the SnRK1 signaling pathway. Plant Physiol 157:160–174

    CAS  PubMed Central  PubMed  Google Scholar 

  • Deprost D, Truong HN, Robaglia C, Meyer C (2005) An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem Biophys Res Commun 326:844–850

    CAS  PubMed  Google Scholar 

  • Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M, Bedu M, Robaglia C, Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–870

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dietrich K, Weltmeier F, Ehlert A, Weiste C, Stahl M, Harter K, Dröge-Laser W (2011) Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. Plant Cell 23:381–395

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dobrenel T, Marchive C, Azzopardi M, Clement G, Moreau M, Sormani R, Robaglia C, Meyer C (2013) Sugar metabolism and the plant target of rapamycin kinase: a sweet operaTOR? Front Plant Sci 4:93

    CAS  PubMed Central  PubMed  Google Scholar 

  • Doksani Y, Wu JY, de Lange T, Zhuang X (2013) Super-resolution fluorescence imaging of telomeres reveal TRF2-dependent Tloop formation. Cell 155:345–356

    CAS  PubMed  Google Scholar 

  • Dowling RJ, Topisirovic I, Alain T, Bidinosti M, Fonseca BD, Petroulakis E, Wang X, Larsson O, Selvaraj A, Liu Y, Kozma SC, Thomas G, Sonenberg N (2010) mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328:1172–1176

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eveland AL, Jackson DP (2013) Sugars, signaling, and plant development. J Exp Bot 63:3367–3377

    Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fujiki Y, Yoshikawa Y, Sato T, Inada N, Ito M, Nishida I, Watanabe A (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol Plant 111:345–352

    CAS  PubMed  Google Scholar 

  • Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102

    CAS  PubMed  Google Scholar 

  • Gomez LD, Gilday A, Feil R, Lunn JE, Graham IA (2010) AtTPS1-mediated trehalose 6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant J 64:1–13

    CAS  PubMed  Google Scholar 

  • Gonzali S, Loreti E, Solfanelli C, Novi G, Alpi A, Perata P (2006) Identification of sugar-modulated genes and evidence for in vivo sugar sensing in Arabidopsis. J Plant Res 119:115–123

    CAS  PubMed  Google Scholar 

  • Granot D (2007) Role of tomato hexose kinases. Functional Plant Biol 34:564–570

    CAS  Google Scholar 

  • Gutierrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari M, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105:4939–4944

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hanson J, Hanssen M, Wiese A, Hendrik MMWB, Smeekens S (2008) The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE2. Plant J 53:935–949

    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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hardie DG, Ross FA, Hawley SA (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nature Rev Mol Cell Biol 13:251–261

    CAS  Google Scholar 

  • Heisel TJ, Li CY, Grey KM, Gibson SI (2013) Mutations in HISTONE ACETYLETRANSFERASE1 affect sugar response and gene expression in Arabidopsis. Front Plant Sci 4:245

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hong YF, Ho THD, Wu CF, Ho SL, Yeh RH, Lu CA, Chen PW, Yu LC, Chao A, Yu SM (2012) Convergent starvation signals and hormone crosstalk in regulating nutrient mobilization upon germination in cereals. Plant Cell 24:2857–2873

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huang Y, Li CY, Biddle KD, Gibson SI (2008) Identification, cloning and characterization of sis7 and sis10 sugar-insensitive mutants of Arabidopsis. BMC Plant Biol 8:104

    PubMed Central  PubMed  Google Scholar 

  • Huang Y, Li CY, Pattison DL, Gray WM, Park S, Gibson SA (2010) SUGAR-INSENSITIVE3, a ring E3 ligase, is a new player in plant sugar response. Plant Physiol 152:1889–1900

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huang Y, Li CY, Park S, Gibson SI (2013) SIS8, as putative mitogenactivated protein kinase kinase kinase, regulates sugar resistant seedling development in Arabidopsis. Plant J doi: 10.1111/tpj.12404

    Google Scholar 

  • Hsu YF, Chen YC, Hsiao YC, Wang BJ, Lin SY, Cheng WH, Jauh GY, Harada JJ, Wang CS (2014) AtRH57, a DEAD-box RNA helicase, is involved in feedback inhibition of glucose-mediated abscisic acid accumulation during seedling development and additively affects pre-ribosomal RNA processing with high glucose. Plant J 77:119–135

    CAS  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    CAS  PubMed  Google Scholar 

  • Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kandel-Kfir M, Damari-Weissler H, German MA, Gidoni D, Mett A, Belausov E, Petreikov M, Adir N, Granot D (2006) Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization. Planta 224:1341–1352

    CAS  PubMed  Google Scholar 

  • Kang SG, Price J, Lin PC, Hong JC, Jang JC (2010) The Arabidopsis bZIP1 transcription factor is involved in sugar signaling, protein networking, and DNA binding. Mol Plant 3:361–373

    CAS  PubMed  Google Scholar 

  • Kang SA, Pacold ME, Cervantes CL, Lim D, Lou HJ, Ottina K, Gray NS, Turk BE, Yaffe MB, Sabatini DM (2013) mTORC1 phosphorylation sites encode their sensitivity to starvation and rapamycin. Science 341:1236566-1–9

    Google Scholar 

  • Karve A, Rauh BL, Xia X, Kandasamy M, Meagher RB, Sheen J, Moore BD (2008) Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta 228:411–425

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karve R, Lauria M, Virnig A, Xia X, Rauh BL, Moore BD (2010) Evolutionary lineages and functional diversification of plant hexokinases. Mol Plant 3:334–346

    CAS  PubMed  Google Scholar 

  • Karve A, Xia X, Moore BD (2012) Arabidopsis hexokinase-like1 and hexokinase1 form a critical node in mediating plant glucose and ethylene responses. Plant Physiol 158:1965–1975

    CAS  PubMed Central  PubMed  Google Scholar 

  • Katsir L, Davies KA, Bergmann DC, Laux T (2011) Peptide signaling in plant development. Curr Biol 21:R356–R364

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kelly G, David-Schartz R, Sade N, /Moshelion M, Levi A, Alchanatis V, Granot D (2012) The pitfalls of transgenic selection and new roles of AtHXK1: a high level of AtHXK1 expression uncouples hexokinas1-dependent sugar signaling from exogenous sugar. Plant Physiol 159:47–51

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keurentjes JJ, Fu J, de Vos CH, Lommen A, Hall RD, Bino RJ, van der Plas LH, Jansen RC, Vreugdenhil D, Koornneef M (2006) The genetics of plant metabolism. Nat Genet 38:842–849

    CAS  PubMed  Google Scholar 

  • Kim M, Lim JH, Shn CS, Park K, Kim GT, Kim WT, Pai HS (2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18:2341–2355

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim YM, Heinzel N, Giese JO, Koeber J, Melzer M, Rutten T, von Wiren N, Sonnewald U, Hajirezaei MR (2013) A dual role of tobacco hexokinase1 in primary metabolism and sugar sensing. Plant Cell Environ 36:1311–1327

    CAS  Google Scholar 

  • Kleinow T, Himbert S, Krenz B, Jeske 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

    CAS  Google Scholar 

  • Laplante M, Sabatini DM (2012) mTOR signaling in growth control and disease. Cell 149:274–293

    CAS  PubMed Central  PubMed  Google Scholar 

  • LeClere S, Schmelz EA, Chourey PS (2010) Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiol 153:306–318

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee KW, Chen PW, Lu CA, Chen S, Ho TH, Yu SM (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61

    PubMed  Google Scholar 

  • Lee H, Chah OK, Plotnikov J, Sheen J (2013) Stem Cell Signaling in Immunity and Development. CSHL Symposium on Quantitative Biology. Online doi:10.1101/sqb.2012.77.014837

    Google Scholar 

  • Leon P, Sheen J (2003) Sugar and hormone connections. Trends in Plant Sci 8:110–116

    CAS  Google Scholar 

  • Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine. Genome Res 16:414–427.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li P, Wind JJ, Shi X, Zhang H, Hanson J, Smeekens SC, Teng S (2011) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci USA 108:3436–3441

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin JF, Wu SH (2004) molecular events in senescing Arabidopsis leaves. Plant J 39:612–628

    CAS  PubMed  Google Scholar 

  • Lin PC, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S, Kamiya Y, Jang JC (2010) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA- and GA-mediated growth, stress and gene expression responses. Plant J 65:253–268

    PubMed  Google Scholar 

  • Liu Y, Bassham DC (2010) TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One 5:e11883

    PubMed Central  PubMed  Google Scholar 

  • Liu Q, Kirubakaran S, Hur W, Niepel M, Westover K, Thoreen CC, Wang J, Ni J, Patricelli MP, Vogel K, Riddle S, Waller DL, Traynor R, Sanda T, Zhao Z, Kang SA, Zhao J, Look AT, Sorger PK, Sabatini DM, Gray NS (2012) Kinome-wide selectivity profiling of ATP-competitive mammalian target of rapamycin (mTOR) inhibitors and characterization of their binding kinetics. J Biol Chem 287:9742–9752

    CAS  PubMed Central  PubMed  Google Scholar 

  • Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perat P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucroseinduced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179:1004–1016

    CAS  PubMed  Google Scholar 

  • Lova A, Sos-Hegedus A, Bimbo A, Banfalvi Z (2003) Functional diversity of potato SNF1-related kinases tested in Saccharomyces cerevisiae. Gene 321:123–129

    Google Scholar 

  • Lu CA, Lin CC, Lee KW, Chen JL, Huang LF, Ho SL, Liu HJ, Hsing YI, Yu SM (2007) The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19:2484–2499

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mahfouz MM, Kim S, Delauney AJ, Verma DP (2006) Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18:477–490

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martin T, Oswald O, Graham IA (2002) Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon:nitrogen availability. Plant Physiol 128:472–481

    CAS  PubMed Central  PubMed  Google Scholar 

  • Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99:6422–6427

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mishra BS, Singh M, Aggrawal P, Laxmi A (2009) Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLOS one 4:e4502

    PubMed Central  PubMed  Google Scholar 

  • Montane MH, Menand B (2013) ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells but no developmental patterning change. J Exp Bot 64:4361–4374

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336

    CAS  PubMed  Google Scholar 

  • Moreau M, Azzopardi M, Clement G, Dobrenel T, Marchive C, Renne C, Martin-Magniette ML, Taconnat L, Renou JP, Robaglia C, Meyer C (2012) 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. Plant Cell 24:463–481

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mudgil Y, Uhrig J, Zhou J, Temple B, Jiang K, Jones AM (2009) Arabidopsis N-MYC DOWNREGULATED-LIKE1, a positive regulator of auxin transport in a G protein-mediated pathway. Plant Cell 21:3591–3609

    CAS  PubMed Central  PubMed  Google Scholar 

  • Naouar N, Vandepoele K, Lammens T, Casneuf T, Zeller G, van Hummelen P, Weigel D, Ratsch G, Inze D, Kuiper M, De Veylder L, Vuylsteke M (2009) Quantitative RNA expression analysis with Affymetrix Tiling 1.0R arrays identifies new E2F target genes. Plant J 57:184–194

    CAS  PubMed  Google Scholar 

  • Ng S, Giraud E, Duncan O, Law SR, Wang Y, Xu L, Narsai R, Carrie C, Walker H, Day DA, Blanco NE, Strand A, Whelan J, Ivanova A (2013) Cyclin-dependnet kinase E1 (CDKE1) provides a cellular switch in plants between growth and stress responses. J Biol Chem 288:3449–3459

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nilsson A, Olsson T, Ulfstedt M, Thelander M, Ronne H (2011) Two novel types of hexokinases in the moss Physcomitrella patens. BMC Plant Biol 11:32

    CAS  PubMed Central  PubMed  Google Scholar 

  • Obertello M, Krouk G, Katari MS, Runko SJ, Coruzzi GM (2010) Modeling the global effect of the basic-leucine zipper transcription factor 1 (bZIP1) on nitrogen and light regulation in Arabidopsis. BMC Sys Biol 4:111

    Google Scholar 

  • Ohto M, Hayashi S, Sawa S, Hashimoto-Ohta A, Nakamura K (2006) Involvement of HLS1 in sugar and auxin signaling in Arabidopsis leaves. Plant Cell Physiol 47:1603–1611

    CAS  PubMed  Google Scholar 

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

    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

    CAS  PubMed Central  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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Purcell PC, Smith AM, Halford NG (1998) Antisense expression of a 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. The Plant J 14:195–202

    CAS  Google Scholar 

  • Radchuk R, Emery RJN, Weier D, Vigeolas H, Geigenberger P, Lunn JE, Feil R, Weschk W, Weber H (2009) Sucrose non-fermenting kinase 1 (SnRK1) coordinates metabolic and hormonal signals during pea cotyledon growth and differentiation. Plant J 61:324–338

    PubMed  Google Scholar 

  • Rahmani F, Hummel M, Schuurmans J, Wiese-Klinkenberg A, Smekens S, Hanson J (2009) Sucrose control of translation mediated by an upstream open reading frame-encoded peptide. Plant Physiol 50:1356–1367

    Google Scholar 

  • Ramon M, Rolland F (2007) Plant development: introducing trehalose metabolism. Trend Plant Sci 12:185–188

    CAS  Google Scholar 

  • Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling in Arabidopsis. The Arabidopsis Book. doi: 10.1199/tab.0117

    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

    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 γsubunit of the plant energy sensor SnRK1. Plant J 75:11–25

    CAS  PubMed  Google Scholar 

  • Ren M, Qiu S, Venglat P, Xiang D, Feng L, Selvaraj G, Datla R (2011) Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol 155:1367–1382

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ren M, Venglat P, Qiu S, Feng L, Cao Y, Wang E, Xiang D, Wang J, Alexander D, Chalivendra S, Logan D, Mattoo A, Selvaraj G, Datla R (2012) Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 24:4850–4874

    CAS  PubMed Central  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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14Suppl:S185–205

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Ryu JY, Jeong SW, Kim SY, Ko Y, Yoon S, Choi SB, Park YI (2008) Cyanobacterial glucokinase complements the glucose sensing role of Arabidopsis thaliana hexkinase1. Bioch Bioph Res Comm 374:454–459

    CAS  Google Scholar 

  • Santner A, Calderon-Villalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301–307

    CAS  PubMed  Google Scholar 

  • Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D (2006) A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441:227–30

    CAS  PubMed  Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sheen J (2010) Discover and connect cellular signaling. Plant Physiol 154:562–566

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schepetilnikov M, Dimitrova M, Mancera-Martinez E, Geldreich A, Keller M, Ryabova LA (2013) TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h. EMBO J 32:1087–1102

    CAS  PubMed  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 Physiology 135:879–890

    CAS  PubMed Central  PubMed  Google Scholar 

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

    PubMed Central  PubMed  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 USA 103:12935–12940

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279

    CAS  PubMed  Google Scholar 

  • Sugden C, Donaghy PG, Halford NG, Hardie DG (1999) 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

    CAS  PubMed Central  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

    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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thimm O, Blasing O, Gibson Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller 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

    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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Urano D, Phan N, Jones JC, Yang J, Huang J, Grigston J, Taylor JP, Jones AM (2012) Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nature Cell Biol 14:1079–1088

    CAS  PubMed Central  PubMed  Google Scholar 

  • Urban J, Soulard A, Huber A, Lippman S, Mukhopadhyay D, Deloche O, Wanke V, Anrather D, Ammerer G, Riezman H, Broach JR, De Virgilio C, Hall MN, Loewith R (2007) Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol Cell 26:663–674

    CAS  PubMed  Google Scholar 

  • Van Dijken AJH, Schluepmann H, Smeekens SCM (2004) Arabidopsis trehalose 6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135:969–77

    PubMed Central  PubMed  Google Scholar 

  • Vandepoele K, Vlieghe K, Florquin K, Hennig L, Beemster GT, Gruissem W, Van de Peer Y, Inze D, De Veylder L (2005) Genome-wide identification of potential plant E2F target genes. Plant Physiol 139:316–328

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Frank A, Feil R, Lunn JE, Stitt M, Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–707

    CAS  PubMed  Google Scholar 

  • Wind, J, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochem 71:1610–1614

    CAS  Google Scholar 

  • Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124:471–484

    CAS  PubMed  Google Scholar 

  • Xiao W, Sheen J, Jang JC (2000) Multiple sugar signal transduction pathways in plants. Plant Mol Biol 44:451–461

    CAS  PubMed  Google Scholar 

  • Xiong Y, Sheen J (2012) Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J Biol Chem 287:2836–2842

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J (2013) Glucose-TOR signaling reprograms the transcriptome and activates meristems. Nature 496:181–186

    CAS  PubMed  Google Scholar 

  • Xiong Y, Sheen J (2013) Moving beyond translation: glucose-TOR signaling in the transcriptional control of cell cycle. Cell Cycle 12:1989–1990

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong Y, Sheen J (2014) The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol 164:499–512

    PubMed  Google Scholar 

  • Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signaling in plants. Nature 425:521–525

    CAS  PubMed  Google Scholar 

  • Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789–795

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yuan HX, Xiong Y, Guan KL (2013) Nutrient sensing, metabolism, and cell growth control. Mol Cell 49:379–387

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Y, Primavesi LF, Jhurreea D, Andraloj 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang ZW, Yaun S, Xu F, Yang H, Zhang NH, Cheng J, Lin HH (2010) The plastid hexokinase pHXK: a node of convergence for sugar and plastid signals in Arabidopsis FEBS Lett 584:3573–3579

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Biology and Centre for Computational and Integrative Biology, Massachusetts General Hospital, and Department of Genetics, Harvard Medical School, Boston, MA, 02114, USA

    Jen Sheen

Authors
  1. Jen Sheen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jen Sheen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sheen, J. Master regulators in plant glucose signaling networks. J. Plant Biol. 57, 67–79 (2014). https://doi.org/10.1007/s12374-014-0902-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-014-0902-7

Keywords

Search

Navigation