Transgenic Research

, Volume 20, Issue 5, pp 1003–1018 | Cite as

Promoter of the AlSAP gene from the halophyte grass Aeluropus littoralis directs developmental-regulated, stress-inducible, and organ-specific gene expression in transgenic tobacco

  • Rania Ben Saad
  • Walid Ben Romdhan
  • Nabil Zouari
  • Jalel Azaza
  • Delphine Mieulet
  • Jean-Luc Verdeil
  • Emmanuel Guiderdoni
  • Afif Hassairi
Original Paper

Abstract

In our recent published work it has been demonstrated that AlSAP, a gene encoding an A20/AN1 zinc-finger protein (stress-associated protein) of the C4 halophyte grass Aeluropuslittoralis, is inducible by various abiotic stresses and by hormonal stimuli. To further investigate the regulation of the gene, a 586-bp genomic fragment upstream of the AlSAP translated sequence has been isolated, cloned, and designated as the “PrAlSAP” promoter. Sequence analysis of “PrAlSAP” revealed the presence of cis-regulatory elements which could be required for abiotic stress, abscisic acid (ABA), and salicylic acid (SA) responsiveness and for tissue-specific and vascular expression. The PrAlSAP promoter was fused to the β-glucuronidase (gusA) gene and the resulting construct transferred into tobacco. Histochemical assays of stably transformed tobacco plants showed that PrAlSAP is active in this heterologous C3 system. While full-length gusA transcripts accumulated in whole 15, 30, and 45-day-old plants, GUS histochemical staining was only observed in leaves and stems of 45-day-old, or older, transgenic seedlings. Histological sections prepared at this stage revealed activity localized in leaf veins (phloem and bundle sheath) and stems (phloem and cortex) but not in roots. Furthermore, gusA transcripts accumulated in an age-dependent manner with a basipetal pattern in leaf and stem tissues throughout the plant. In flowers, GUS expression was detected in sepals only. The accumulation of gusA transcripts was up-regulated by salt, dehydration, ABA, and SA treatment. Altogether, these results show that, when used in a heterologous dicot system, PrAlSAP is an age-dependent, abiotic-stress-inducible, organ-specific and tissue-specific promoter.

Keywords

Aeluropus littoralis PrAlSAP promoter AlSAP Abiotic stresses Transgenic tobacco 

Notes

Acknowledgments

The authors are grateful to S. Abid a teacher of English, for the English revision. Part of this work was conducted under the REFUGE platform funded by Agropolis Foundation, Montpellier France. This study was supported by a grant from the Ministry of Higher Education Scientific Research of Tunisia (contract program 2006–2010) and by the European project CEDROME (FP6-INCO-CT-2005-015468).

Supplementary material

11248_2010_9474_MOESM1_ESM.tif (69 kb)
Online Resource 1 The third High-Efficiency Thermal Asymmetric Interlaced (HE-TAIL) PCR for 5′-flanking sequence of AlSAP gene. M: DNA Ladder; lanes 1, 2 and 3: products of the tertiary PCR using Rn2-ZFRv3, Rn2-ZFRv4 and Rn2-Rn2 primers, respectively (TIFF 68 kb)
11248_2010_9474_MOESM2_ESM.tif (56 kb)
Online Resource 2 Southern blot analysis of transgenic lines (L4, L6, L8 and L12). Genomic DNA was extracted, digested with NcoI (cuts once in the T-DNA) and loaded onto the gel which was blotted and probed with labeled PCR product of gusA gene (TIFF 56 kb)

References

  1. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868PubMedCrossRefGoogle Scholar
  2. Behnam B, Kikuchi A, Toprak FC, Yamanaka S, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN (2006) The Arabidopsis DREB1A gene driven by the stress-inducible rd29A promoter increases salt-stress tolerance in proportion to its copy number in tetrasomic tetraploid potato (Solanum tuberosum). Plant Biotech 23:169–177. doi:10.1007/s00299-007-0360-5 CrossRefGoogle Scholar
  3. Ben Saad R, Zouari N, Ben Ramdhan W, Azaza J, Meynard D, Guiderdoni E, Hassairi A (2010) Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger “AlSAP” gene isolated from the halophyte grass Aeluropus littoralis. Plant Mol Biol 72:171–190. doi:10.1007/s11103-009-9560-4 PubMedCrossRefGoogle Scholar
  4. Branco-Price C, Kawaguchi RB, Ferreira J, Bailey-Serres J (2005) Genome wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660. doi:10.1093/aob/mci217 PubMedCrossRefGoogle Scholar
  5. Chen H, Nelson RS, Sherwood JL (1994) Enhanced recovery of transformants of Agrobacterium tumifaciens after freeze-thaw transformation and drug selection. Biotechniques 16:664–668PubMedGoogle Scholar
  6. Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18:675–689PubMedCrossRefGoogle Scholar
  7. Colot V, Robert LS, Kavanagh TA, Bevan MW, Thompson RD (1987) Localization of sequences in wheat endosperm protein genes which confer tissue-specific expression in tobacco. EMBO J 6:3559–3564PubMedGoogle Scholar
  8. Cornejo MJ, Luth D, Blankenship KM, Anderson OD, Blechl AE (1993) Activity of a maize ubiquitin promoter in transgenic rice. Plant Mol Biol 23:567–581. doi:0176-1617/03/160/10-1233 PubMedCrossRefGoogle Scholar
  9. De Valck D, Heyninck K, Van Criekinge W, Contreras R, Beyaert R, Fiers W (1996) A20, an inhibitor of cell death, self-associates by its zinc finger domain. FEBS Lett 384:61–64. doi:10.1016/0014-5793(96)00283-9 PubMedCrossRefGoogle Scholar
  10. De Valck D, Jin DY, Heyninck K, Van de Craen M, Contreras R, Fiers W, Jeang KT, Beyaert R (1999) The zinc finger protein A20 interacts with a novel anti-apoptotic protein which is cleaved by specific caspases. Oncogene 18:4182–4190PubMedCrossRefGoogle Scholar
  11. Evans PC, Ovaa H, Hamon M, Kilshaw PE, Hamm S, Bauer S, Ploegh HL, Smith TS (2004) Zinc-finger protein A20, a regulator of inflammation and cell survival, has de-ubiquitinating activity. Biochem J 378:727–734. doi:10.1042/BJ20031377 PubMedCrossRefGoogle Scholar
  12. Floris M, Mahgoub H, Lanet E, Robaglia C, Menand B (2009) Post-transcriptional regulation of gene expression in plants during abiotic stress. Int J Mol Sci 10:3168–3185. doi:10.3390/ijms10073168 PubMedCrossRefGoogle Scholar
  13. Gao SQ, Chen M, Ma YZ (2005) Activity of rd29A promoter in wheat immature embryonic calli. Acta Agron Sin 31:150–153Google Scholar
  14. Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress-tolerant and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81PubMedCrossRefGoogle Scholar
  15. Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16:1077–1090. doi:10.1105/tpc.019729 PubMedCrossRefGoogle Scholar
  16. Guo L, Yu Y, Xia X, Yin W (2010) Identification and functional characterisation of the promoter of the calcium sensor gene CBL1 from the xerophyte Ammopiptanthus mongolicus. BMC Plant Biol 29:10–18. doi:10.1186/1471-2229-10-18 Google Scholar
  17. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300PubMedCrossRefGoogle Scholar
  18. Hood EE, Gelvin SB, Melchers S, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plant. Transgenic Res 2:208–218. doi:10.1007/BF01977351 CrossRefGoogle Scholar
  19. Horsch RB, Fry J, Hoffmann N, Neidermeyer J, Rogers SG, Fraley RT (1988) Leaf disc transformation. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual. Kluwer Academic Publishers, Dordrecht, pp 1–9Google Scholar
  20. Hsieh TH, Lee JT, Charng YY, Chan MT (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130:618–626. doi:10.1104/pp.003442 PubMedCrossRefGoogle Scholar
  21. Hua XJ, Van de Cotte B, Van Montagu M, Verbruggen N (2001) The 5′ untranslated region of the At-P5R gene is involved in both transcriptional and post-transcriptional regulation. Plant J 26:157–169PubMedCrossRefGoogle Scholar
  22. Huang J, Wang MM, Jiang Y, Bao YM, Huang X, Sun H, Xu DQ, Lan HX, Zhang HS (2008) Expression analysis of rice A20/AN1-type zinc finger genes and characterization of ZFP177 that contributes to temperature stress tolerance. Gene 420:135–144. doi:10.1016/j.gene.2008.05.019 PubMedCrossRefGoogle Scholar
  23. Hudson ME, Quail PH (2003) Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 133:1605–1616. doi:10.1104/pp.103.030437 PubMedCrossRefGoogle Scholar
  24. 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 47:141–153. doi:10.1093/pcp/pci230 PubMedCrossRefGoogle Scholar
  25. Iwamoto M, Higo H, Higo K (2004) Strong expression of the rice catalase gene CatB promoter in protoplasts and roots of both monocots and dicots. Plant Physiol Biochem 42:241–249. doi:10.1016/j.plaphy.2004.01.008 PubMedCrossRefGoogle Scholar
  26. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907. doi:10.1007/BF02667740 PubMedGoogle Scholar
  27. Jin Y, Wang M, Fu J, Xuan N, Zhu Y, Lian Y, Jia Z, Zheng J, Wang G (2007) Phylogenetic and expression analysis of ZnF-AN1 genes in plants. Genomics 90:265–275. doi:10.1016/j.ygeno.2007.03.019 PubMedCrossRefGoogle Scholar
  28. Kanneganti V, Gupta AK (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol 66:445–462. doi:10.1007/s11103-007-9284-2 PubMedCrossRefGoogle Scholar
  29. Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in arabidopsis. Plant Cell 18:2733–2748. doi:10.1105/tpc.106.042713 PubMedCrossRefGoogle Scholar
  30. Karim S et al (2007) Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol 64:371–386. doi:10.1007/s11103-007-9159-6 PubMedCrossRefGoogle Scholar
  31. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291. doi:10.1038/7036 PubMedCrossRefGoogle Scholar
  32. Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350PubMedCrossRefGoogle Scholar
  33. Kawaguchi R, Bailey-Serres J (2002) Regulation of translational initiation in plants. Curr Opin Plant Biol 5:460–465. doi:10.1016/S1369-5266(02)00290-X PubMedCrossRefGoogle Scholar
  34. Ke J, Choi JK, Smith M, Horner HT, Nikolau BJ, Wurtele ES (1997) Structure of the CAC1 gene and in situ characterization of its expression (the arabidopsis thaliana gene coding for the biotin-containing subunit of the plastidic acetyl-coenzyme a carboxylase). Plant Physiol 113:357–365PubMedCrossRefGoogle Scholar
  35. Kurek I, Stoger E, Dulberger R, Christou P, Breiman A (2002) Overexpression of the wheat FK506-binding protein 73 (FKBP73) and the heat-induced wheat FKBP77 in transgenic wheat reveals different functions of the two isoforms. Transgenic Res 11:373–379PubMedCrossRefGoogle Scholar
  36. Lacombe E, Van Doorsselaere J, Boerjan W, Boudet AM, Grima-Pettenati J (2000) Characterization of cis-elements required for vascular expression of the cinnamoyl CoA reductase gene and for protein-DNA complex formation. Plant J 23:663–676. doi:10.1046/j.1365-313x.2000.00838.x PubMedCrossRefGoogle Scholar
  37. Lam E, Chua NH (1989) ASF-2: a factor that binds to the cauliflower mosaic virus 35S promoter and a conserved GATA motif in cab promoters. Plant Cell 1:1147–1156PubMedCrossRefGoogle Scholar
  38. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP, Ma A (2000) Failure to regulate TNF-induced NF-κB and cell death responses in A20-deficient mice. Science 289:2350–2354. doi:10.1126/science.289.5488.2350 PubMedCrossRefGoogle Scholar
  39. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327PubMedCrossRefGoogle Scholar
  40. Liu ZZ, Wang JL, Huang X, Xu WH, Liu ZM, Fang RX (2003) The promoter of a rice glycine-rich protein gene, Osgrp-2, confers vascular-specific expression in transgenic plants. Planta 216:824–833. doi:10.1007/s00425-002-0934-y PubMedGoogle Scholar
  41. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods 25:402–408. doi:10.1006/meth.2001.1262 PubMedCrossRefGoogle Scholar
  42. Matzke AJ, Stoger EM, Schernthaner JP, Matzke MA (1990) Deletion analysis of a zein gene promoter in transgenic tobacco plants. Plant Mol Biol 14:323–332PubMedCrossRefGoogle Scholar
  43. Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: when post-transcriptional and post translational regulations control transcription. Plant Sci 174:420–431. doi:10.1016/j.plantsci.2008.02.005 CrossRefGoogle Scholar
  44. McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2:163–171PubMedCrossRefGoogle Scholar
  45. Michiels A, Tucker M, Van den Ende W, Van Laere A (2003a) Chromosomal walking of flanking regions from short known sequences in GC-rich plant genomic DNA. Plant Mol Biol Report 21:295–302CrossRefGoogle Scholar
  46. Michiels A, Van den Ende W, Tucker M, Van Riet L, Van Laere A (2003b) Extraction of high-quality genomic DNA from latex-containing plants. Anal Biochem 315:85–89. doi:10.1016/S0003-2697(02)00665-6 PubMedCrossRefGoogle Scholar
  47. Mohanty B, Krishnan SP, Swarup S, Bajic VB (2005) Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species. Ann Bot (Lond) 96:669–681CrossRefGoogle Scholar
  48. Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314. doi:10.1073/pnas.0401572101 PubMedCrossRefGoogle Scholar
  49. Nishiuchi T, Shinshi H, Suzuki K (2004) Rapid and transient activation of transcription of the ERF3 gene by wounding in tobacco leaves: possible involvement of NtWRKYs and autorepression. J Biol Chem 279:55355–55361. doi:10.1074/jbc.M409674200 PubMedCrossRefGoogle Scholar
  50. Odell JT, Nagy F, Chua NH (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:810–812PubMedCrossRefGoogle Scholar
  51. Park HC et al (2004) Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol 135:2150–2161. doi:10.1104/pp.104.041442 PubMedCrossRefGoogle Scholar
  52. Pino MT, Skinner JS, Park EJ, Jeknic Z, Hayes PM, Thomashow MF, Chen TH (2007) Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield. Plant Biotechnol J 5:591–604. doi:10.1111/j.1467-7652.2007.00269.x PubMedCrossRefGoogle Scholar
  53. Planchais S, Perennes C, Glab N, Mironov V, Inze D, Bergounioux C (2002) Characterization of cis-acting element involved in cell cycle phase-independent activation of Arath;CycB1;1 transcription and identification of putative regulatory proteins. Plant Mol Biol 50:111–127PubMedCrossRefGoogle Scholar
  54. Quattrocchio F, Tolk MA, Coraggio I, Mol JN, Viotti A, Koes RE (1990) The maize zein gene zE19 contains two distinct promoters which are independently activated in endosperm and anthers of transgenic Petunia plants. Plant Mol Biol 15:81–93PubMedCrossRefGoogle Scholar
  55. Ramsperger VC, Summers RG, Berry JO (1996) Photosynthetic gene expression in meristems and during initial leaf development in a C4 dicotyledonous plant. Plant Physiol 111:999–1010PubMedGoogle Scholar
  56. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  57. Schernthaner JP, Matzke MA, Matzke JM (1988) Endosperm-specific activity of a zein gene promoter in transgenic tobacco plants. EMBO J 7:1249–1255PubMedGoogle Scholar
  58. Scott DA et al (1998) Identification and mutation analysis of a cochlear-expressed, zinc finger protein gene at the DFNB7/11 and dn hearing-loss-loci on human chromosome 9q and mouse chromosome19. Gene 215:461–469. doi:10.1016/S0378-1119(98)00316-3 PubMedCrossRefGoogle Scholar
  59. Sheen J (1999) C4 gene expression. Annu Rev Plant Physiol Plant Mol Biol 50:187–217PubMedCrossRefGoogle Scholar
  60. Shi H, Kim Y, Guo Y, Stevenson B, Zhu JK (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15:19–32. doi:10.1105/tpc.007872 PubMedCrossRefGoogle Scholar
  61. Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270. doi:10.1046/j.1365-313X.2003.01624.x PubMedCrossRefGoogle Scholar
  62. Sinha NR, Williams RE, Hake S (1993) Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7:787–795. doi:10.1101/gad.7.5.787 PubMedCrossRefGoogle Scholar
  63. Sun XH, Chen MJ (2002) A brief account of promoter cloning. Acta Edulis Fungi 9:57–62Google Scholar
  64. Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54:582–596. doi:10.1007/s000180050186 PubMedCrossRefGoogle Scholar
  65. Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46:445–474. doi:10.1146/annurev.pp.46.060195.002305 CrossRefGoogle Scholar
  66. Tittarelli A et al (2007) Isolation and comparative analysis of the wheat TaPT2 promoter: identification in silico of new putative regulatory motifs conserved between monocots and dicots. J Exp Bot 58:2573–2582. doi:10.1093/jxb/erm123 PubMedCrossRefGoogle Scholar
  67. Tjaden G, Edwards JW, Coruzzi GM (1995) cis elements and trans-acting factors affecting regulation of a nonphotosynthetic light-regulated gene for chloroplast glutamine synthetase. Plant Physiol 108:1109–1117PubMedCrossRefGoogle Scholar
  68. Uknes S, Dincher S, Friedrich L, Negrotto D, Williams S, Thompson-Taylor H, Potter S, Ward E, Ryals J (1993) Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell 5:159–169. doi:10.1105/tpc.5.2.159 PubMedCrossRefGoogle Scholar
  69. Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539. doi:10.1073/pnas.190309197 PubMedCrossRefGoogle Scholar
  70. Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger(s) in rice and their phylogenetic relationship with Arabidopsis. Mol Genet Genomics 276:565–575. doi:10.1007/s00438-006-0165-1 PubMedCrossRefGoogle Scholar
  71. Vij Sh, Tyagi AK (2008) A20/AN1 zinc-finger domain-containing proteins in plants and animals represent common elements in stress response. Funct Integr Genomics 8:301–307. doi:10.1007/s10142-008-0078-7 PubMedCrossRefGoogle Scholar
  72. Wilkie GS, Dickson KS, Gray NK (2003) Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci 28:182–188PubMedCrossRefGoogle Scholar
  73. Wu Y, Zhou H, Que YX, Chen RK, Zhang MQ (2008) Cloning and identification of promoter Prd29A and its application in sugarcane drought resistance. Sugar Tech 10:36–41CrossRefGoogle Scholar
  74. Xu XM, Meier I (2008) The nuclear pore comes to the fore. Trends Plant Sci 13:20–27. doi:10.1016/j.tplants.2007.12.001 PubMedCrossRefGoogle Scholar
  75. Xu R, Zhao H, Dinkins RD, Cheng X, Carberry G, Li QQ (2006) The 73 kD subunit of the cleavage and polyadenylation specificity factor (CPSF) complex affects reproductive development in Arabidopsis. Plant Mol Biol 61:799–815. doi:10.1007/s11103-006-0051-6 PubMedCrossRefGoogle Scholar
  76. Yanagisawa S, Schmidt RJ (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J 17:209–214. doi:10.1046/j.1365-313X.1999.00363 PubMedCrossRefGoogle Scholar
  77. Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058. doi:10.1074/jbc.M207941200 PubMedCrossRefGoogle Scholar
  78. Zhang ZL, Xie Z, Zou X, Casaretto J, Ho TH, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513. doi:10.1104/pp.103.034967 PubMedCrossRefGoogle Scholar
  79. Zhang N, Si HJ, Wang D (2005) Cloning of rd29A gene promoter from arabidopsis thaliana and its application in stress-resistance transgenic potato. Acta Agron Sin 31:159–164. doi:10.1007/s12355-008-0006-0 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Rania Ben Saad
    • 1
  • Walid Ben Romdhan
    • 1
  • Nabil Zouari
    • 1
  • Jalel Azaza
    • 1
  • Delphine Mieulet
    • 2
  • Jean-Luc Verdeil
    • 2
  • Emmanuel Guiderdoni
    • 2
  • Afif Hassairi
    • 1
    • 3
  1. 1.University of Sfax, Centre of Biotechnology of Sfax (CBS)SfaxTunisia
  2. 2.CIRAD, UMR DAPMontpellier Cedex5France
  3. 3.King Saud University, CEBRRiyadhSaudi Arabia

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