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Plant Molecular Biology Reporter

, Volume 29, Issue 1, pp 209–216 | Cite as

Isolation, Phylogeny and Expression Patterns of AP2-Like Genes in Apple (Malus × domestica Borkh)

  • Jing Zhuang
  • Quan-Hong Yao
  • Ai-Sheng Xiong
  • Jian Zhang
Article

Abstract

The AP2/ERF family transcription factors (TFs) act as the nodes of a regulatory network in a plant's response to abiotic and biotic stress. AP2-like genes from apple (Malus × domestica Borkh), one of the most widely cultivated fruit trees worldwide, were identified and analysed in order to understand the transcriptional regulation through the AP2/ERF family TFs. Starting from the M. domestica database, 58 AP2-like TFs were identified by in silico cloning using the AP2/ERF TFs amino acid sequence of Arabidopsis thaliana as a probe. The AP2/ERF TFs from apple were classified into four subfamilies, DREB, ERF, AP2 and RAV. To establish detailed expression data of this gene family in apple, six kinds of tissue (bud, flower, fruit, leaf, root and stem) and cell culture were examined for the presence of AP2-like genes. Most of the apple AP2-like genes indicate some degree of tissue specificity and were most abundant in root followed by stem, and expression levels were low in leaf and in bud.

Keywords

Transcription factor AP2/ERF Phylogeny Expression profile Arabidopsis thaliana Malus × domestica Borkh 

Notes

Acknowledgements

The research was supported by the International Scientific and Technological Cooperation of Canada–China (Shanghai–Alberta); Hi-tech Research and Development Program of China (2006AA10Z117); National key Project of Transgenic Crops of China (2009ZX08002-011B); Shanghai Rising-Star Program and Natural Science Foundation (08QH14021, 08ZR1417200).

Supplementary material

11105_2010_227_MOESM1_ESM.doc (97 kb)
Supplementary Table S1 The apple AP2/ERF family member expression profiles suggested by analysis of EST counts based UniGene (Transcripts per millon (TPM). (/: means the cDNA Sources from mixed whole plant) (DOC 97 kb)
11105_2010_227_MOESM2_ESM.doc (134 kb)
Supplementary Figure S1 Comparison of deduced amino acid sequences of the AP2 DNA-binding domains of the AP2 subfamily proteins from A. thaliana and M. domestica. The black background represents conserved amino acid residues in each group. (DOC 134 kb)
11105_2010_227_MOESM3_ESM.doc (104 kb)
Supplementary Figure S2 Comparison of deduced amino acid sequences of the AP2 and B3 DNA-binding domains of the RAV subfamily proteins from A. thaliana and M. domestica. The black background represents conserved amino acid residues in each group. (DOC 104 kb)
11105_2010_227_MOESM4_ESM.doc (371 kb)
Supplementary Figure S3 The classification of AP2/ERF family factors among A. thaliana, O. sativa, V. vinifera and M. domestica. The size of each piece is proportional to the relative abundance to the AP2/ERF genes assigned to this group. (DOC 371 kb)
11105_2010_227_MOESM5_ESM.doc (348 kb)
Supplementary Figure S4 The deduced amino acid sequence alignment of the AP2/ERF DNA-binding domain of ERF subfamily proteins from apple in this study and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 348 kb)
11105_2010_227_MOESM6_ESM.doc (309 kb)
Supplementary Figure S5 The deduced amino acid sequences alignment of the AP2/ERF DNA-binding domain of DREB subfamily proteins from apple in this study and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 309 kb)
11105_2010_227_MOESM7_ESM.doc (106 kb)
Supplementary Figure S6 Comparison of full length of deduced amino acid sequences of the ERF-B1 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 106 kb)
11105_2010_227_MOESM8_ESM.doc (62 kb)
Supplementary Figure S7 Comparison of full length of deduced amino acid sequences of the ERF-B2 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 62 kb)
11105_2010_227_MOESM9_ESM.doc (114 kb)
Supplementary Figure S8 Comparison of full length of deduced amino acid sequences of the ERF-B3 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 114 kb)
11105_2010_227_MOESM10_ESM.doc (62 kb)
Supplementary Figure S9 Comparison of full length of deduced amino acid sequences of the ERF-B4 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 62 kb)
11105_2010_227_MOESM11_ESM.doc (56 kb)
Supplementary Figure S10 Comparison of full length of deduced amino acid sequences of the ERF-B5 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 56 kb)
11105_2010_227_MOESM12_ESM.doc (110 kb)
Supplementary Figure S11 Comparison of full length of deduced amino acid sequences of the ERF-B6 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 110 kb)
11105_2010_227_MOESM13_ESM.doc (42 kb)
Supplementary Figure S12 Comparison of full length of deduced amino acid sequences of the DREB-A1 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 42 kb)
11105_2010_227_MOESM14_ESM.doc (89 kb)
Supplementary Figure S13 Comparison of full length of deduced amino acid sequences of the DREB-A4 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 89 kb)
11105_2010_227_MOESM15_ESM.doc (69 kb)
Supplementary Figure S14 Comparison of full length of deduced amino acid sequences of the DREB-A5 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 69 kb)
11105_2010_227_MOESM16_ESM.doc (77 kb)
Supplementary Figure S15 Comparison of full length of deduced amino acid sequences of the DREB-A6 group proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 77 kb)
11105_2010_227_MOESM17_ESM.doc (49 kb)
Supplementary Figure S16 Comparison of full length of deduced amino acid sequences of the RAV subfamily proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 49 kb)
11105_2010_227_MOESM18_ESM.doc (114 kb)
Supplementary Figure S17 Comparison of full length of deduced amino acid sequences of the AP2 subfamily proteins from apple and Arabidopsis. The black background represents conserved amino acid residues in each group. (DOC 114 kb)
11105_2010_227_MOESM19_ESM.doc (27 kb)
Supplementary Figure S18 Tissue-specific expression of the apple DREB subfamily genes. (DOC 27 kb)
11105_2010_227_MOESM20_ESM.doc (27 kb)
Supplementary Figure S19 Tissue-specific expression of the apple AP2 and RAV subfamily genes. (DOC 27 kb)

References

  1. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274CrossRefPubMedGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedGoogle Scholar
  3. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  4. Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424CrossRefPubMedGoogle Scholar
  5. Chen WJ, Zhu T (2004) Networks of transcription factors with roles in environmental stress response. Trends Plant Sci 9:591–596CrossRefPubMedGoogle Scholar
  6. Chen L, Zhang Z, Liang H, Liu H, Du L, Xu H, Xin Z (2008) Overexpression of TiERF1 enhances resistance to sharp eyespot in transgenic wheat. J Exp Bot 59:4195–4204CrossRefPubMedGoogle Scholar
  7. Chen M, Xu Z, Xia L, Li L, Cheng X, Dong J, Wang Q, Ma Y (2009) Cold-induced modulation and functional analyses of the DRE-binding transcription factor gene, GmDREB3, in soybean (Glycine max L). J Exp Bot 60:121–135CrossRefPubMedGoogle Scholar
  8. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500CrossRefPubMedGoogle Scholar
  9. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG (2003) OsDREB genes in rice, Oryza sativa L, encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763CrossRefPubMedGoogle Scholar
  10. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427CrossRefPubMedGoogle Scholar
  11. Espley RV, Brendolise C, Chagné D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten HJ, Gardiner SE, Hellens RP, Allan AC (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell 21:168–183CrossRefPubMedGoogle Scholar
  12. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788CrossRefPubMedGoogle Scholar
  13. Gil-Humanes J, Pistón F, Martín A, Barro F (2009) Comparative genomic analysis and expression of the APETALA2-like genes from barley, wheat, and barley–wheat amphiploids. BMC Plant Biol 29:66CrossRefGoogle Scholar
  14. Guo A, He K, Liu D, Bai S, Gu X (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21:2568–2569CrossRefPubMedGoogle Scholar
  15. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471CrossRefPubMedGoogle Scholar
  16. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877CrossRefPubMedGoogle Scholar
  17. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153CrossRefPubMedGoogle Scholar
  18. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467CrossRefPubMedGoogle Scholar
  19. James DJ, Passey AJ, Barbara DJ, Bevan M (1989) Genetic transformation of apple (Malus pumila Mill) using a disarmed Ti-binary vector. Plant Cell Rep 7:658–661Google Scholar
  20. Kazuko YS, Kazuo S (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefGoogle Scholar
  21. Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189CrossRefPubMedGoogle Scholar
  22. Li Y, Su X, Zhang B, Huang Q, Zhang X, Huang R (2009) Expression of jasmonic ethylene responsive factor gene in transgenic poplar tree leads to increased salt tolerance. Tree Physiol 29:273–279CrossRefPubMedGoogle Scholar
  23. Mitsuda N, Ohme-Takagi M (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol 50:1232–1248CrossRefPubMedGoogle Scholar
  24. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432CrossRefPubMedGoogle Scholar
  25. Navarro M, Marque G, Ayax C, Keller G, Borges JP, Marque C, Teulières C (2009) Complementary regulation of four eucalyptus CBF genes under various cold conditions. J Exp Bot 60:2713–2724CrossRefPubMedGoogle Scholar
  26. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95CrossRefPubMedGoogle Scholar
  27. Potter D, Eriksson T, Evans RC, Oh SH, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault MP, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266:5–43CrossRefGoogle Scholar
  28. Qin QL, Liu JG, Zhang Z, Peng RH, Xiong AS (2007) Isolation, optimization, and functional analysis of the cDNA encoding transcription factor RdreB1 in Oryza sativa L. Mol Breed 19:329–340CrossRefGoogle Scholar
  29. Riano PDM, Ruzicic S, Dreyer I, Mueller RB (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinform 8:42CrossRefGoogle Scholar
  30. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646CrossRefPubMedGoogle Scholar
  31. Sakuma Y, Liu Q, Dubouzet JG, Abe H, 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
  32. Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436CrossRefPubMedGoogle Scholar
  33. Takos AM, Jaffé FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232CrossRefPubMedGoogle Scholar
  34. 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
  35. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U (2006) The genome of black cottonwood, Populus trichocarpa (Torr & Gray). Science 313:1596–1604CrossRefPubMedGoogle Scholar
  36. Yamaguchi SK, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefGoogle Scholar
  37. Yang TW, Zhang LJ, Zhang TG, Zhang H, Xu SJ (2005) Transcriptional regulation network of cold-responsive genes in higher plants. Plant Sci 169:987–995CrossRefGoogle Scholar
  38. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B (2002) A draft sequence of the rice genome (Oryza sativa L ssp indica). Science 296:79–92CrossRefPubMedGoogle Scholar
  39. Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L). J Exp Bot 59:4095–4107CrossRefPubMedGoogle Scholar
  40. Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796CrossRefPubMedGoogle Scholar
  41. 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 Commun 371:468–474CrossRefPubMedGoogle Scholar
  42. Zhuang J, Peng RH, Cheng ZM, Zhang J, Cai B, Zhang Z, Gao F, Zhu B, Fu XY, Jin XF, Chen JM, Qiao YS, Xiong AS, Yao QH (2009) Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera. Sci Hortic 123:73–81CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Shanghai Academy of Agricultural SciencesShanghaiChina
  2. 2.Alberta Innovates-Technology Futures/Alberta Research CouncilVegrevilleCanada

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