Protoplasma

, Volume 245, Issue 1–4, pp 3–14 | Cite as

AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling

  • Karl-Josef Dietz
  • Marc Oliver Vogel
  • Andrea Viehhauser
Review Article

Abstract

To optimize acclimation responses to environmental growth conditions, plants integrate and weigh a diversity of input signals. Signal integration within the signalling networks occurs at different sites including the level of transcription factor activation. Accumulating evidence assigns a major and diversified role in environmental signal integration to the family of APETALA 2/ethylene response element binding protein (AP2/EREBP) transcription factors. Presently, the Plant Transcription Factor Database 3.0 assigns 147 gene loci to this family in Arabidopsis thaliana, 200 in Populus trichocarpa and 163 in Oryza sativa subsp. japonica as compared to 13 to 14 in unicellular algae (http://plntfdb.bio.uni-potsdam.de/v3.0/). AP2/EREBP transcription factors have been implicated in hormone, sugar and redox signalling in context of abiotic stresses such as cold and drought. This review exemplarily addresses present-day knowledge of selected AP2/EREBP with focus on a function in stress signal integration and retrograde signalling and defines AP2/EREBP-linked gene networks from transcriptional profiling-based graphical Gaussian models. The latter approach suggests highly interlinked functions of AP2/EREBPs in retrograde and stress signalling.

Keywords

AP2/EREBP Gaussian models Transcription factors Hormone Redox Retrograde signalling Abiotic stress 

Abbreviations

ABA

abscisic acid

AP2

APETALA 2

DCMU

3-(3,4-dichlorophenyl)-1,1-dimethylurea

CBF

C-repeat binding factor

DREB

dehydration-responsive element binding protein

EREBP

ethylene response element binding protein

ERF

ethylene responsive factor

GGM

graphical Gaussian model

PSY

phytoene synthase

RAP2

related to AP2

RAV

related to ABI3/VP1

TF

transcription factor

Supplementary material

709_2010_142_MOESM1_ESM.doc (398 kb)
Supplementary Table 1List of all AP2/EREBP transcription factors from A. thaliana. The table compiles gene identification number, classification, size and assigned names according to TAIR and UniProt (Jain et al. 2009, Swarbreck et al. 2008, The Uniprot Consortium 2009) (DOC 397 kb)
709_2010_142_MOESM2_ESM.doc (456 kb)
Supplementary Table 2List of genes assigned to graphical Gaussian models (GGM). Table lists names and annotations for genes co-expressed with specified “seed genes”, namely At1g19210, At1g21910, At1g22190, At1g33760, At1g36060, At1g43160, At1g79700, ABI4, At3g14230, At3g50260, At4g34410, At4g39780, At5g18560, At5g47220, At5g51190 and At5g52020. (DOC 455 kb)

References

  1. Baier M, Ströher E, Dietz KJ (2004) The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant Cell Physiol 45:997–1006CrossRefPubMedGoogle Scholar
  2. Brazhnik P, de la Fuente A, Mendes P (2002) Gene networks: how to put the function in genomics. Trends Biotechnol 20:467–472CrossRefPubMedGoogle Scholar
  3. Büttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci USA 94:5961–5966CrossRefPubMedGoogle Scholar
  4. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743CrossRefPubMedGoogle Scholar
  5. Chung S, Parish RW (2008) Combinatorial interactions of multiple cis-elements regulating the induction of the Arabidopsis XERO2 dehydrin gene by abscisic acid and cold. Plant J 54:15–29CrossRefPubMedGoogle Scholar
  6. Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468CrossRefPubMedGoogle Scholar
  7. Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002CrossRefPubMedGoogle Scholar
  8. Feng JX, Liu D, Pan Y, Gong W, Ma LG, Luo JC, Deng XW, Zhu YX (2005) An annotation update via cDNA sequence analysis and comprehensive profiling of developmental, hormonal or environmental responsiveness of the Arabidopsis AP2/EREBP transcription factor gene family. Plant Mol Biol 59:853–868CrossRefPubMedGoogle Scholar
  9. Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054CrossRefPubMedGoogle Scholar
  10. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690CrossRefPubMedGoogle Scholar
  11. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404CrossRefPubMedGoogle Scholar
  12. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442CrossRefPubMedGoogle Scholar
  13. Guo HW, Ecker JR (2004) The ethylene signaling pathway: new insights. Current Opinion Plant Biol 7:40–49CrossRefGoogle Scholar
  14. Heber U, Lange OL, Shuvalov VA (2006) Conservation and dissipation of light energy as complementary processes: homoiohydric and poikilohydric autotrophs. J Exp Bot 57:1211–1223CrossRefPubMedGoogle Scholar
  15. Horling F, Lamkemeyer P, Konig J, Finkemeier I, Kandlbinder A, Baier M, Dietz KJ (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiology 131:317–325CrossRefPubMedGoogle Scholar
  16. Iwase A, Matsui K, Ohme-Takagi M (2009) Manipulation of plant metabolic pathways by transcription factors. Plant Biotechnol 26:29–38Google Scholar
  17. Jain E, Bairoch A, Duvaud S, Phan I, Redaschi N, Suzek BE, Martin MJ, McGarvey P, Gasteiger E (2009) Infrastructure for the life sciences: design and implementation of the UniProt website. BMC Bioinformatics 10:136CrossRefPubMedGoogle Scholar
  18. Jofuku KD, Denboer BGW, van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene apetala 2. Plant Cell 6:1211–1225CrossRefPubMedGoogle Scholar
  19. Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 27:470–478CrossRefPubMedGoogle Scholar
  20. Karim MR, Hirota A, Kwiatkowska D, Tasaka M, Aida M (2009) A role for Arabidopsis PUCHI in floral meristem identity and bract suppression. Plant Cell 21:1360–1372CrossRefPubMedGoogle Scholar
  21. Khandelwal A, Elvitigala T, Ghosh B, Quatrano RS (2008) Arabidopsis transcriptome reveals control circuits regulating redox homeostasis and the role of an AP2 transcription factor. Plant Physiol 148:2050–2058CrossRefPubMedGoogle Scholar
  22. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Multiple signals from damaged chloroplasts converge on a common pathway to regulate nuclear gene expression. Science 316:715–719, Title according to erratum as to 2007-6-22CrossRefPubMedGoogle Scholar
  23. Krizek BA (2009) AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol 150:1916–1929CrossRefPubMedGoogle Scholar
  24. Lin RC, Park HJ, Wang HY (2008) Role of Arabidopsis RAP2.4 in regulating light- and ethylene-mediated developmental processes and drought stress tolerance. Mol Plant 1:42–57CrossRefPubMedGoogle Scholar
  25. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406CrossRefPubMedGoogle Scholar
  26. Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178CrossRefPubMedGoogle Scholar
  27. Ma S, Bohnert HJ (2008) Gene networks in Arabidopsis thaliana for metabolic and environmental functions. Mol Biosyst 4:199–204CrossRefPubMedGoogle Scholar
  28. Ma S, Gong Q, Bohnert HJ (2007) An Arabidopsis gene network based on the graphical Gaussian model. Genome Res 17:1614–1625CrossRefPubMedGoogle Scholar
  29. Magnani E, Sjölander K, Hake S (2004) From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell 16:2265–2277CrossRefPubMedGoogle Scholar
  30. Manfield IW, Jen CH, Pinney JW, Michalopoulos I, Bradford JR, Gilmartin PM, Westhead DR (2006) Arabidopsis Co-expression Tool (ACT): web server tools for microarray-based gene expression analysis. Nucleic Acids Res 34:W504–W509CrossRefPubMedGoogle Scholar
  31. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tilling array. Plant Cell Phys 49(8):1135–1149CrossRefGoogle Scholar
  32. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182CrossRefPubMedGoogle Scholar
  33. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081CrossRefPubMedGoogle Scholar
  34. Riano-Pachon DM, Ruzicic S, Dreyer I, Mueller-Roeber B (2007) plnTFDB: an integrative plant transcription factor database. BMC Bioinformatics 8:42CrossRefPubMedGoogle Scholar
  35. Richly E, Dietzmann A, Biehl A, Kurth J, Laloi C, Apel K, Salamini F, Leister D (2003) Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch. EMBO reports 4(5):491–498CrossRefPubMedGoogle Scholar
  36. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736–11743CrossRefPubMedGoogle Scholar
  37. Rook F, Bevan MW (2003) Genetic approaches to understanding sugar-response pathways. J Exp Bot 54:495–501CrossRefPubMedGoogle Scholar
  38. Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant Journal 26:421–433CrossRefPubMedGoogle Scholar
  39. Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29:426–434CrossRefPubMedGoogle Scholar
  40. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  41. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009CrossRefPubMedGoogle Scholar
  42. Sauter A, Dietz KJ, Hartung W (2002) A possible stress physiological role of abscisic acid conjugates in root-to-shoot signalling. Plant Cell and Environment 25:223–228CrossRefGoogle Scholar
  43. Schäfer J, Strimmer K (2005) A shrinkage approach to large-scale covariance matrix estimation and implications for functional genomics. Stat Appl Genet Mol Biol 4:32Google Scholar
  44. Schwacke R, Fischer K, Ketelsen B, Krupinska K, Krause K (2007) Comparative survey of plastid and mitochondrial targeting properties of transcription factors in Arabidopsis and rice. Mol Genet Genomics 277:631–646CrossRefPubMedGoogle Scholar
  45. Shaikhali J, Heiber I, Seidel T, Ströher E, Hiltscher H, Birkmann S, Dietz KJ, Baier M (2008) The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes. BMC Plant Biol 8:48CrossRefPubMedGoogle Scholar
  46. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Current Opinion Plant Biol 3:217–223Google Scholar
  47. Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396CrossRefPubMedGoogle Scholar
  48. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040CrossRefPubMedGoogle Scholar
  49. Ströher E, Dietz KJ (2006) Concepts and approaches towards understanding the cellular redox proteome. Plant Biol 8:407–418CrossRefPubMedGoogle Scholar
  50. Sun S, Yu JP, Chen F, Zhao TJ, Fang XH, Li YQ, Sui SF (2008) TINY, a dehydration-responsive element (DRE)-binding protein-like transcription factor connecting the DRE- and ethylene-responsive element-mediated signaling pathways in Arabidopsis. J Biol Chem 283:6261–6271CrossRefPubMedGoogle Scholar
  51. Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014CrossRefPubMedGoogle Scholar
  52. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  53. Toh H, Horimoto K (2002) Inference of a genetic network by a combined approach of cluster analysis and graphical Gaussian modeling. Bioinformatics 18:287–297CrossRefPubMedGoogle Scholar
  54. The UniProt Consortium (2009) The Universal Protein Resource (UniProt). Nucleic Acids Res 37:D169–D174CrossRefGoogle Scholar
  55. Voigt C, Oster U, Börnke F, Jahns P, Dietz KJ, Leister D, Kleine T (2010) In-depth analysis of the distinctive effects of norflurazon implies that tetrapyrrole biosynthesis, organellar gene expression and ABA cooperate in the GUN-type of plastid signalling. Physiol Plant 138:503–519Google Scholar
  56. Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frey NFD, Leung J (2008) An update on abscisic acid signaling in plants and more. Molecular Plant 1:198–217CrossRefPubMedGoogle Scholar
  57. Weigel D (1995) The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell 7:388–389CrossRefPubMedGoogle Scholar
  58. Wellmer F, Riechmann JL (2005) Gene network analysis in plant development by genomic technologies. Int J Dev Biol 49:745–759CrossRefPubMedGoogle Scholar
  59. Welsch R, Medina J, Giuliano G, Beyer P, Von Lintig J (2003) Structural and functional characterization of the phytoene synthase promoter from Arabidopsis thaliana. Planta 216:523–534PubMedGoogle Scholar
  60. Welsch R, Maass D, Voegel T, Dellapenna D, Beyer P (2007) Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol 145:1073–1085CrossRefPubMedGoogle Scholar
  61. Wilson K, Long D, Swinburne J, Coupland G (1996) A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8:659–671CrossRefPubMedGoogle Scholar
  62. Zhuang J, Cai B, Peng RH, Zhu B, Jin XF, Xue Y, Gao F, Fu XY, Tian YS, Zhao W, Qiao YS, Zhang Z, Xiong AS, Yao QH (2008) Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem Biophys Res Com 371:468–474CrossRefPubMedGoogle Scholar
  63. Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40:22–34CrossRefPubMedGoogle Scholar
  64. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Karl-Josef Dietz
    • 1
  • Marc Oliver Vogel
    • 1
  • Andrea Viehhauser
    • 1
  1. 1.Biochemistry and Physiology of Plants–W5Bielefeld UniversityBielefeldGermany

Personalised recommendations