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PMID: 18701338 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S. Review

Convergent energy and stress signaling.

Trends in plant science ·Vol. 13 ·No. 9 ·2008-09-00 ·Pages 474-82

Baena-González E, Sheen J

Abstract

Plants are constantly confronted by multiple types of stress. Despite their distinct origin and mode of perception, nutrient deprivation and most stresses have an impact on the overall energy status of the plant, leading to convergent downstream responses that include largely overlapping transcriptional patterns. The emerging view is that this transcriptome reprogramming in energy and stress signaling is partly regulated by the evolutionarily conserved energy sensor protein kinases, SNF1 (sucrose non-fermenting 1) in yeast, AMPK (AMP-activated protein kinase) in mammals and SnRK1 (SNF1-related kinase 1) in plants. Upon sensing the energy deficit associated with stress, nutrient deprivation and darkness, SnRK1 triggers extensive transcriptional changes that contribute to restoring homeostasis, promoting cell survival and elaborating longer-term responses for adaptation, growth and development.

MeSH Terms
Adaptation, Physiological Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Darkness Energy Metabolism Gene Expression Regulation, Plant Homeostasis Protein Serine-Threonine Kinases/genetics,metabolism Receptor Cross-Talk Signal Transduction
Chemicals
Arabidopsis Proteins Protein Serine-Threonine Kinases SnRK1 protein, Arabidopsis
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Baena-González Elena
Department of Genetics, Harvard Medical School, Boston, MA 02114, USA.
Sheen Jen
References (79)
79 references, click to expand
  1. 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. 2003 Feb;54(383):739-47 PMID: 12554717
  2. Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars.
    Physiol Plant. 2001 Mar;111(3):345-352 PMID: 11240919
  3. Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3747-52 PMID: 10725385
  4. 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. 1999 May;120(1):257-74 PMID: 10318703
  5. 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. 1999 Aug;19(4):433-9 PMID: 10504565
  6. Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression.
    Genome Biol. 2007;8(4):R49 PMID: 17408486
  7. 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. 2006 Jan;140(1):263-78 PMID: 16361518
  8. Specific in vitro phosphorylation of plant eIF2alpha by eukaryotic eIF2alpha kinases.
    Plant Mol Biol. 1999 Oct;41(3):363-70 PMID: 10598103
  9. Mechanical stress induces biotic and abiotic stress responses via a novel cis-element.
    PLoS Genet. 2007 Oct;3(10):1800-12 PMID: 17953483
  10. Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose.
    Plant J. 2006 Jul;47(2):211-23 PMID: 16771775
  11. The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice.
    Plant Cell. 2007 Aug;19(8):2484-99 PMID: 17766403
  12. Sucrose is a signal molecule in assimilate partitioning.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4784-8 PMID: 9539816
  13. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots.
    Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12935-40 PMID: 16912118
  14. Translational control by TOR and TAP42 through dephosphorylation of eIF2alpha kinase GCN2.
    Genes Dev. 2003 Apr 1;17(7):859-72 PMID: 12654728
  15. A central integrator of transcription networks in plant stress and energy signalling.
    Nature. 2007 Aug 23;448(7156):938-42 PMID: 17671505
  16. Regulatory functions of nuclear hexokinase1 complex in glucose signaling.
    Cell. 2006 Nov 3;127(3):579-89 PMID: 17081979
  17. The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation.
    EMBO Rep. 2007 Sep;8(9):864-70 PMID: 17721444
  18. Functional identification of an Arabidopsis snf4 ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast.
    Plant J. 2000 Jul;23(1):115-22 PMID: 10929106
  19. CARBOHYDRATE-MODULATED GENE EXPRESSION IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540 PMID: 15012299
  20. SNF1/AMPK pathways in yeast.
    Front Biosci. 2008 Jan 01;13:2408-20 PMID: 17981722
  21. Antisense repression of StubGAL83 affects root and tuber development in potato.
    Plant J. 2003 Jan;33(1):139-47 PMID: 12943548
  22. Functional diversity of potato SNF1-related kinases tested in Saccharomyces cerevisiae.
    Gene. 2003 Dec 4;321:123-9 PMID: 14636999
  23. Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate.
    Plant Physiol. 2000 May;123(1):403-12 PMID: 10806257
  24. Coordination of carbon supply and plant growth.
    Plant Cell Environ. 2007 Sep;30(9):1126-49 PMID: 17661751
  25. Coping with stress: eIF2 kinases and translational control.
    Biochem Soc Trans. 2006 Feb;34(Pt 1):7-11 PMID: 16246168
  26. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings.
    Plant J. 2007 Feb;49(3):463-91 PMID: 17217462
  27. Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development.
    Plant J. 2007 Mar;49(6):1053-63 PMID: 17286797
  28. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
    Plant J. 2004 Mar;37(6):914-39 PMID: 14996223
  29. The plasticity of aging: insights from long-lived mutants.
    Cell. 2005 Feb 25;120(4):449-60 PMID: 15734678
  30. Autophagy in development and stress responses of plants.
    Autophagy. 2006 Jan-Mar;2(1):2-11 PMID: 16874030
  31. AMPK and transcriptional regulation.
    Front Biosci. 2008 Jan 01;13:3022-33 PMID: 17981775
  32. Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression.
    Mol Cell Biol. 2000 Jul;20(13):4513-21 PMID: 10848578
  33. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis.
    Plant J. 2005 May;42(4):567-85 PMID: 15860015
  34. SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control?
    Trends Plant Sci. 2007 Jan;12(1):20-8 PMID: 17166759
  35. Transcriptomic adaptations in rice suspension cells under sucrose starvation.
    Plant Mol Biol. 2007 Mar;63(4):441-63 PMID: 17115300
  36. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses.
    Plant J. 2007 Apr;50(2):347-63 PMID: 17376166
  37. Molecular cloning of an arabidopsis homologue of GCN2, a protein kinase involved in co-ordinated response to amino acid starvation.
    Planta. 2003 Aug;217(4):668-75 PMID: 12905023
  38. Insulin and amino-acid regulation of mTOR signaling and kinase activity through the Rheb GTPase.
    Oncogene. 2006 Oct 16;25(48):6361-72 PMID: 17041622
  39. Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants.
    Genome Biol. 2004;5(11):R91 PMID: 15535867
  40. Cellular and genetic responses of plants to sugar starvation.
    Plant Physiol. 1999 Nov;121(3):687-93 PMID: 10557216
  41. Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions.
    Plant Physiol. 2004 Sep;136(1):2734-46 PMID: 15333755
  42. AKINbetagamma contributes to SnRK1 heterotrimeric complexes and interacts with two proteins implicated in plant pathogen resistance through its KIS/GBD sequence.
    Plant Physiol. 2006 Nov;142(3):931-44 PMID: 17028154
  43. A conserved upstream open reading frame mediates sucrose-induced repression of translation.
    Plant Cell. 2004 Jul;16(7):1717-29 PMID: 15208401
  44. NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation.
    J Exp Bot. 2008;59(3):667-80 PMID: 18296429
  45. Structural basis for AMP binding to mammalian AMP-activated protein kinase.
    Nature. 2007 Sep 27;449(7161):496-500 PMID: 17851531
  46. The Arabidopsis CDPK-SnRK superfamily of protein kinases.
    Plant Physiol. 2003 Jun;132(2):666-80 PMID: 12805596
  47. AtVPS34, a phosphatidylinositol 3-kinase of Arabidopsis thaliana, is an essential protein with homology to a calcium-dependent lipid binding domain.
    Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11398-402 PMID: 7972072
  48. Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation.
    Plant Physiol. 2004 Aug;135(4):2330-47 PMID: 15310832
  49. Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene.
    Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6422-7 PMID: 11983923
  50. Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5322-7 PMID: 10220464
  51. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis.
    Plant Cell. 2005 Dec;17(12):3257-81 PMID: 16299223
  52. Sugar sensing and signaling in plants: conserved and novel mechanisms.
    Annu Rev Plant Biol. 2006;57:675-709 PMID: 16669778
  53. The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness.
    Plant J. 2006 Sep;47(5):751-60 PMID: 16923016
  54. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply.
    Plant Cell. 2002 Sep;14(9):2191-213 PMID: 12215515
  55. The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation.
    Plant Cell. 2005 Sep;17(9):2587-600 PMID: 16055629
  56. Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells.
    Proc Natl Acad Sci U S A. 2008 Jan 29;105(4):1380-5 PMID: 18216250
  57. Autophagic recycling: lessons from yeast help define the process in plants.
    Curr Opin Plant Biol. 2005 Apr;8(2):165-73 PMID: 15752997
  58. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis.
    Plant Cell. 2004 Aug;16(8):2128-50 PMID: 15273295
  59. The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis.
    Plant Cell. 2006 Apr;18(4):893-906 PMID: 16517759
  60. Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine.
    Genome Res. 2006 Mar;16(3):414-27 PMID: 16424108
  61. Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period.
    Plant J. 2004 Sep;39(6):847-62 PMID: 15341628
  62. Snf1-related protein kinase 1 is needed for growth in a normal day-night light cycle.
    EMBO J. 2004 Apr 21;23(8):1900-10 PMID: 15057278
  63. Large-scale analysis of mRNA translation states during sucrose starvation in arabidopsis cells identifies cell proliferation and chromatin structure as targets of translational control.
    Plant Physiol. 2006 Jun;141(2):663-73 PMID: 16632591
  64. Expression and evolutionary features of the hexokinase gene family in Arabidopsis.
    Planta. 2008 Aug;228(3):411-25 PMID: 18481082
  65. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy.
    Nat Rev Mol Cell Biol. 2007 Oct;8(10):774-85 PMID: 17712357
  66. Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis.
    Plant Cell Physiol. 2007 Mar;48(3):405-13 PMID: 17234672
  67. 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. 2003 Aug;35(4):490-500 PMID: 12904211
  68. The SOS3 family of calcium sensors and SOS2 family of protein kinases in Arabidopsis.
    Plant Physiol. 2004 Mar;134(3):919-26 PMID: 15020756
  69. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling.
    Science. 2003 Apr 11;300(5617):332-6 PMID: 12690200
  70. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks.
    Curr Opin Plant Biol. 2006 Aug;9(4):436-42 PMID: 16759898
  71. Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase.
    J Exp Bot. 2003 Jan;54(382):467-75 PMID: 12508057
  72. Autophagy regulates programmed cell death during the plant innate immune response.
    Cell. 2005 May 20;121(4):567-577 PMID: 15907470
  73. Highly conserved protein kinases involved in the regulation of carbon and amino acid metabolism.
    J Exp Bot. 2004 Jan;55(394):35-42 PMID: 14645392
  74. THE MOLECULAR-GENETICS OF NITROGEN ASSIMILATION INTO AMINO ACIDS IN HIGHER PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:569-593 PMID: 15012301
  75. Molecular events in senescing Arabidopsis leaves.
    Plant J. 2004 Aug;39(4):612-28 PMID: 15272878
  76. Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase.
    Plant Cell. 2003 Apr;15(4):1034-48 PMID: 12671096
  77. Remodeling of yeast genome expression in response to environmental changes.
    Mol Biol Cell. 2001 Feb;12(2):323-37 PMID: 11179418
  78. Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes.
    Plant Physiol. 2008 Apr;146(4):1834-61 PMID: 18305208
  79. Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana.
    J Biol Chem. 2004 Oct 1;279(40):41758-66 PMID: 15292193
Article Info
Journal
Trends in plant science
Abbr.
Trends Plant Sci
ISSN
1360-1385
DOI
10.1016/j.tplants.2008.06.006
Published
2008-09-00
Epub
2008-00-11
Pages
474-82
Language
English
Region
England
NLM ID
9890299
PMCID
PMC3075853
Subset
IM
Grants
NIGMS NIH HHS · R01 GM060493 · United States
NIGMS NIH HHS · R01 GM060493-08 · United States
External Links
PubMed source DOI: 10.1016/j.tplants.2008.06.006 PMC Full Text View journal details
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