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PMID: 12953112 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter.

The Plant cell ·Vol. 15 ·No. 9 ·2003-09-00 ·Pages 2076-92

Sun C, Palmqvist S, Olsson H, Borén M, Ahlandsberg S, Jansson C

Abstract

SURE (sugar responsive) is a cis element in plant sugar signaling. The SURE element was reported first for potato, in which it confers sugar responsiveness to the patatin promoter. A SURE binding transcription factor has not been isolated. We have isolated a transcription factor cDNA from barley and purified the corresponding protein. The transcription factor, SUSIBA2 (sugar signaling in barley), belongs to the WRKY proteins and was shown to bind to SURE and W-box elements but not to the SP8a element in the iso1 promoter. Nuclear localization of SUSIBA2 was demonstrated in a transient assay system with a SUSIBA2:green fluorescent protein fusion protein. Exploiting the novel transcription factor oligodeoxynucleotide decoy strategy with transformed barley endosperm provided experimental evidence for the importance of the SURE elements in iso1 transcription. Antibodies against SUSIBA2 were produced, and the expression pattern for susiba2 was determined at the RNA and protein levels. It was found that susiba2 is expressed in endosperm but not in leaves. Transcription of susiba2 is sugar inducible, and ectopic susiba2 expression was obtained in sugar-treated leaves. Likewise, binding to SURE elements was observed for nuclear extracts from sugar-treated but not from control barley leaves. The temporal expression of susiba2 in barley endosperm followed that of iso1 and endogenous sucrose levels, with a peak at approximately 12 days after pollination. Our data indicate that SUSIBA2 binds to the SURE elements in the barley iso1 promoter as an activator. Furthermore, they show that SUSIBA2 is a regulatory transcription factor in starch synthesis and demonstrate the involvement of a WRKY protein in carbohydrate anabolism. Orthologs to SUSIBA2 were isolated from rice and wheat endosperm.

MeSH Terms
Amino Acid Sequence Base Sequence Carbohydrates/pharmacology Cloning, Molecular DNA, Complementary/chemistry,genetics DNA-Binding Proteins/genetics,metabolism Escherichia coli/genetics Gene Expression Regulation, Plant/drug effects Hordeum/genetics,metabolism Molecular Sequence Data Nuclear Localization Signals/genetics,metabolism Oryza/genetics,metabolism Plant Proteins/genetics,metabolism Promoter Regions, Genetic/genetics Protein Binding Recombinant Proteins/chemistry,isolation & purification,metabolism Response Elements/genetics Seeds/genetics,metabolism Sequence Analysis, DNA Sequence Analysis, Protein Sequence Homology, Amino Acid Sequence Homology, Nucleic Acid Signal Transduction/genetics Sucrose/metabolism Transcription Factors/genetics,metabolism Triticum/genetics,metabolism
Chemicals
Carbohydrates DNA, Complementary DNA-Binding Proteins Nuclear Localization Signals Plant Proteins Recombinant Proteins SPF1 protein, plant Transcription Factors Sucrose
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Sun Chuanxin
Department of Plant Biology and Forestry Genetics, The Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden.
Palmqvist Sara
Olsson Helena
Borén Mats
Ahlandsberg Staffan
Jansson Christer
References (55)
55 references, click to expand
  1. Storekeeper defines a new class of plant-specific DNA-binding proteins and is a putative regulator of patatin expression.
    Plant J. 2002 May;30(4):489-97 PMID: 12028578
  2. SUGAR-INDUCED SIGNAL TRANSDUCTION IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:49-81 PMID: 15012186
  3. Therapeutic applications of transcription factor decoy oligonucleotides.
    J Clin Invest. 2000 Nov;106(9):1071-5 PMID: 11067859
  4. 5' deletion of a gbss1 promoter region from wheat leads to changes in tissue and developmental specificities.
    Plant Mol Biol. 2002 Aug;49(6):669-82 PMID: 12081374
  5. An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene.
    Proc Natl Acad Sci U S A. 1988 Oct;85(19):7089-93 PMID: 2902624
  6. Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue.
    Plant Cell Physiol. 2002 Jul;43(7):718-25 PMID: 12154134
  7. Glucose repression in yeast.
    Curr Opin Microbiol. 1999 Apr;2(2):202-7 PMID: 10322167
  8. Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5' upstream regions of genes coding for sporamin and beta-amylase from sweet potato.
    Mol Gen Genet. 1994 Sep 28;244(6):563-71 PMID: 7969025
  9. Analyses of isoamylase gene activity in wild-type barley indicate its involvement in starch synthesis.
    Plant Mol Biol. 1999 Jun;40(3):431-43 PMID: 10437827
  10. Identification of an Spl-like element within the immunoglobulin kappa 3' enhancer necessary for maximal enhancer activity.
    Biochemistry. 1996 Jul 2;35(26):8662-9 PMID: 8679628
  11. One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose.
    Mol Gen Genet. 1990 Oct;224(1):136-46 PMID: 1703626
  12. A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes.
    Plant J. 2001 Oct;28(2):123-33 PMID: 11722756
  13. The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley.
    Plant Physiol. 1998 Sep;118(1):37-49 PMID: 9733524
  14. Starch granules: structure and biosynthesis.
    Int J Biol Macromol. 1998 Aug;23(2):85-112 PMID: 9730163
  15. Sucrose regulation of ADP-glucose pyrophosphorylase subunit genes transcript levels in leaves and fruits.
    Plant Sci. 2002 Feb;162(2):239-44 PMID: 11989489
  16. Molecular cloning and characterization of two novel isoforms of the small subunit of ADPglucose pyrophosphorylase from sweet potato.
    Mol Gen Genet. 1997 Mar 26;254(2):179-85 PMID: 9108280
  17. Sugars as signaling molecules.
    Curr Opin Plant Biol. 1999 Oct;2(5):410-8 PMID: 10508760
  18. Sensing trehalose biosynthesis in plants.
    Plant J. 1998 Apr;14(2):143-6 PMID: 9628011
  19. Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley.
    Plant Mol Biol. 2002 Mar-Apr;48(5-6):551-73 PMID: 11999834
  20. Expression of a chimaeric granule-bound starch synthase-GUS gene in transgenic potato plants.
    Plant Mol Biol. 1991 Oct;17(4):691-9 PMID: 1912493
  21. High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5' and 3' flanking sequences and the leader intron.
    Plant Cell. 1995 Sep;7(9):1387-94 PMID: 8589623
  22. The biosynthesis of starch granules.
    Biomacromolecules. 2001 Summer;2(2):335-41 PMID: 11749190
  23. Sugar-responsible elements in the promoter of a gene for beta-amylase of sweet potato.
    Plant Mol Biol. 2001 Jul;46(5):627-37 PMID: 11516155
  24. Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response.
    Plant Mol Biol. 2003 Jan;51(1):21-37 PMID: 12602888
  25. Isolation of an efficient actin promoter for use in rice transformation.
    Plant Cell. 1990 Feb;2(2):163-71 PMID: 2136633
  26. The WRKY superfamily of plant transcription factors.
    Trends Plant Sci. 2000 May;5(5):199-206 PMID: 10785665
  27. The nuclear factor SP8BF binds to the 5'-upstream regions of three different genes coding for major proteins of sweet potato tuberous roots.
    Plant Mol Biol. 1992 Jan;18(1):97-108 PMID: 1531033
  28. Identification of cis-acting elements important for expression of the starch-branching enzyme I gene in maize endosperm.
    Plant Physiol. 1999 Sep;121(1):225-36 PMID: 10482678
  29. Separate cis sequences and trans factors direct metabolic and developmental regulation of a potato tuber storage protein gene.
    Plant J. 1994 Jun;5(6):815-26 PMID: 8054988
  30. The energetics of specific binding of AT-hooks from HMGA1 to target DNA.
    J Mol Biol. 2003 Mar 21;327(2):393-411 PMID: 12628246
  31. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell?
    Annu Rev Biochem. 1998;67:821-55 PMID: 9759505
  32. An M-CAT binding factor and an RSRF-related A-rich binding factor positively regulate expression of the alpha-cardiac myosin heavy-chain gene in vivo.
    Mol Cell Biol. 1994 Aug;14(8):5056-65 PMID: 8035789
  33. Cloning and expression analysis of a potato cDNA that encodes branching enzyme: evidence for co-expression of starch biosynthetic genes.
    Mol Gen Genet. 1991 Nov;230(1-2):39-44 PMID: 1745241
  34. cis- and trans-acting regulatory elements of the yeast URA3 promoter.
    Mol Cell Biol. 1990 Oct;10(10):5257-70 PMID: 2204810
  35. Light-responsive and transcription-enhancing elements regulate the plastid psbD core promoter.
    EMBO J. 1995 Aug 1;14(15):3721-30 PMID: 7641691
  36. Recent progress toward understanding biosynthesis of the amylopectin crystal.
    Plant Physiol. 2000 Apr;122(4):989-97 PMID: 10759494
  37. ENDOSPERM DEVELOPMENT: Cellularization and Cell Fate Specification.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:233-267 PMID: 11337398
  38. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster.
    Cell. 1986 Aug 15;46(4):521-30 PMID: 3015418
  39. 'SPKK' motifs prefer to bind to DNA at A/T-rich sites.
    EMBO J. 1989 Dec 20;8(13):4189-95 PMID: 2556263
  40. Nucleotide Sequence of a Soybean Vegetative Storage Protein vspB Gene.
    Plant Physiol. 1992 Feb;98(2):794-5 PMID: 16668717
  41. SNF1-related protein kinases: global regulators of carbon metabolism in plants?
    Plant Mol Biol. 1998 Jul;37(5):735-48 PMID: 9678569
  42. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998-9002 PMID: 2461560
  43. A cDNA encoding a putative SPF1-type DNA-binding protein from cucumber.
    Gene. 1997 Feb 7;185(2):265-9 PMID: 9055825
  44. Sugar sensing and signaling in plants.
    Plant Cell. 2002;14 Suppl:S185-205 PMID: 12045277
  45. Sugar-inducible expression of a gene for beta-amylase in Arabidopsis thaliana.
    Plant Physiol. 1995 Mar;107(3):895-904 PMID: 7716246
  46. Nucleocytoplasmic transport.
    Science. 1996 Mar 15;271(5255):1513-8 PMID: 8599106
  47. Sugar response element enhances wound response of potato proteinase inhibitor II promoter in transgenic tobacco.
    Plant Mol Biol. 1991 Nov;17(5):973-83 PMID: 1932687
  48. Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes.
    EMBO J. 1996 Oct 15;15(20):5690-700 PMID: 8896462
  49. Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling.
    Plant J. 2001 May;26(4):421-33 PMID: 11439129
  50. Nuclear import and export of proteins in plants: a tool for the regulation of signalling.
    Planta. 2001 Aug;213(4):499-517 PMID: 11556782
  51. Construction of expression vectors based on the rice actin 1 (Act1) 5' region for use in monocot transformation.
    Mol Gen Genet. 1991 Dec;231(1):150-60 PMID: 1753941
  52. High-level expression of tuberous root storage protein genes of sweet potato in stems of plantlets grown in vitro on sucrose medium.
    Plant Mol Biol. 1990 Apr;14(4):595-604 PMID: 2102838
  53. Application of transcription factor "decoy" strategy as means of gene therapy and study of gene expression in cardiovascular disease.
    Circ Res. 1998 Jun 1;82(10):1023-8 PMID: 9622154
  54. Characterization of a tobacco gene encoding a pollen-specific polygalacturonase.
    Plant Mol Biol. 1994 May;25(2):283-97 PMID: 8018876
  55. A polymorphic bipartite motif signals nuclear targeting of early auxin-inducible proteins related to PS-IAA4 from pea (Pisum sativum).
    Plant J. 1995 Jul;8(1):87-96 PMID: 7655509
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.014597
Published
2003-09-00
Pages
2076-92
Language
English
Region
England
NLM ID
9208688
PMCID
PMC181332
Subset
IM
Databases
GENBANK
AY323206, AY324392, AY324393
External Links
PubMed source DOI: 10.1105/tpc.014597 PMC Full Text View journal details
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