Advertisement

Plant Molecular Biology

, 62:195 | Cite as

A novel cis-acting element, ESP, contributes to high-level endosperm-specific expression in an oat globulin promoter

  • Claudia E. VickersEmail author
  • Gangping Xue
  • Peter M. Gresshoff
Original Paper

Abstract

To examine the genetic controls of endosperm (ES) specificity, several cereal seed storage protein (SSP) promoters were isolated and studied using a transient expression analysis system. An oat globulin promoter (AsGlo1) capable of driving strong ES-specific expression in barley and wheat was identified. Progressive 5′ deletions and cis element mutations demonstrated that the mechanism of specificity in the AsGlo1 promoter was distinct from that observed in glutelin and prolamin promoters. A novel interrupted palindromic sequence, ACATGTCATCATGT, was required for ES specificity and substantially contributed to expression strength of the␣AsGlo1 promoter. This sequence was termed the endosperm specificity palindrome (ESP) element. The GCN4 element, which has previously been shown to be required for ES specificity in cereal SSP promoters, had a quantitative role but was not required for tissue specificity. The 960-bp AsGlo1 promoter and a 251-bp deletion containing the ESP element also drove ES-specific expression in stably transformed barley. Reporter gene protein accumulated at very high levels (10% of total soluble protein) in ES tissues of plants transformed with an AsGlo1:GFP construct. Expression strength and tissue specificity were maintained over five transgenic generations. These attributes make the AsGlo1 promoter an ideal promoter for biotechnology applications. In conjunction with previous findings, our data demonstrate that there is more than one genetically distinct mechanism by which ES specificity can be achieved in cereal SSP promoters, and also suggest that there is redundancy between transcriptional and post-transcriptional tissue specificity mechanisms in cereal globulin genes.

Keywords

AsGlo1 promoter ESP element Endosperm specificity GCN4 box Globulin promoter Promoter analysis 

Abbreviations

ABA

abscisic acid

Act1

rice actin gene

AsGlo1

oat 12S globulin gene

bZIP

basic leucine zipper protein

DAP

days after pollination

ES

endosperm

ESP

endosperm specificity palindrome

GA

gibberellin

GFP

green fluorescent protein

GluB-1

rice B1 glutelin gene

Glu-B1

wheat high-molecular weight glutenin gene

GP

Hordeum vulgare cv. Golden Promise

GUSPlus

modified Staphylococcus sp. β-glucuronidase

Hor2-4

barley B1 hordein gene

Hor3−1

barley D hordein gene

SSP

seed storage protein

sUTR

synthetic untranslated leader

TC

tissue culture

TEP

total extractable protein

TSP

total soluble protein

XYN

xylanase

Notes

Acknowledgments

This research was supported by an Australian Government Grains Research and Development Corporation grant (to CEV). The authors wish to thank Stephen Mudge (CSIRO Plant Industry, Brisbane) and Diana Buzas (ARC Centre for Integrative Legume Research, The University of Queensland, Brisbane) for technical advice, Adrian Elliott (Bureau of Sugar Experimental Stations, Brisbane, Australia) for donation of partially purified s65tGFP, Danial Bishop (CSIRO Plant Industry, Canberra) for assistance in generating transgenic barley and Joan Vickers (The University of Southern Queensland, Toowoomba) for useful comments during manuscript preparation.

References

  1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78PubMedCrossRefGoogle Scholar
  2. Albani D, Hammond-Kosack-Michael CU, Smith C, Conlan S, Colot V, Holdsworth M, Bevan MW (1997) The wheat transcriptional activator SPA: A seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9:171–184PubMedCrossRefGoogle Scholar
  3. Anderson OD, Greene FC (1989) The characterization and comparative analysis of high-molecular-weight glutenin genes from genomes A and B of a hexaploid bread wheat. Theor Appl Genet 77:689–700CrossRefGoogle Scholar
  4. Bagga S, Sutton D, Kemp JD, Sengupta-Gopalan C (1992) Constitutive expression of the β-phaseolin gene in different tissues of transgenic alfalfa does not ensure phaseolin accumulation in non-seed tissue. Plant Mol Biol 19:951–958PubMedCrossRefGoogle Scholar
  5. Barker SJ, Harada JJ, Goldberg RB (1988) Cellular localization of soybean storage protein mRNA in transformed tobacco seeds. Proc Natl Acad Sci USA 85:458–462PubMedCrossRefADSGoogle Scholar
  6. Bäumlein H, Nagy I, Villarroel R, Inzé D, Wobus U (1992) Cis-analysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. Plant J 2:233–239PubMedGoogle Scholar
  7. Blechl AE, Lorens GF, Greene FC, Mackey BE, Anderson OD (1994) A transient assay for promoter activity of wheat seed storage protein genes and other genes expressed in developing endosperm. Plant Sci 102: 69–80CrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  9. Chandrasekharan MB, Bishop KJ, Hall TC (2003). Module-specific regulation of the β-phaseolin promoter during embryogenesis. Plant J 33:853–866PubMedCrossRefGoogle Scholar
  10. Chang SJ, Wang ZY, Hong MM (2002) Rice bZIP protein, REB, interacts with GCN4 motif in promoter of Waxy gene. Sci China Ser C-Life Sci 45:352–360CrossRefGoogle Scholar
  11. Cho MJ, Choi HW, Buchanan BB, Lemaux PG (1999a) Inheritance of tissue-specific expression of barley hordein promoter-uidA fusions in transgenic barley plants. Theor Appl Genet 98:1253–1262CrossRefGoogle Scholar
  12. Cho MJ, Wong LH, Marx C, Jiang W, Lemaux PG, Buchanan BB (1999b) Overexpression of thioredoxin h leads to enhanced activity of starch debranching enzyme (pullulanase) in barley grain. Proc Natl Acad Sci USA 96:14641–14646CrossRefADSGoogle Scholar
  13. Cho M-J, Choi H-W, Jiang W, Ha CD, Lemaux PG (2002). Endosperm-specific expression of green fluorescent protein driven by the hordein promoter is stably inherited in transgenic barley (Hordeum vulgare) plants. Physiol Plant 115:144–151PubMedCrossRefGoogle Scholar
  14. de Pater S, Katagiri F, Kijne J, Chua NH (1994) bZIP proteins bind to a palindromic sequence without an ACGT core located in a seed-specific element of the pea lectin promoter. Plant J 6:133–140PubMedCrossRefGoogle Scholar
  15. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  16. Doyle JJ, Schuler MA, Godette WD, Zenger V, Beachy RN, Slightom JL (1986) The glycosylated seed storage proteins of Glycine max and Phaseolus vulgaris: structural homologies of genes and proteins. J Biol Chem 261:9228–9238PubMedGoogle Scholar
  17. Ellerström M, Stålberg K, Ezcurra I, Rask L (1996) Functional dissection of a napin gene promoter: identification of promoter elements required for embryo and endosperm-specific transcription. Plant Mol Biol 32:1019–1027PubMedCrossRefGoogle Scholar
  18. Entwistle J, Knudsen S, Müller M, Cameron-Mills V (1991) Amber codon suppression: the in vivo and in vitro analysis of two C-hordein genes from barley. Plant Mol Biol 17:1217–1231PubMedCrossRefGoogle Scholar
  19. Ericson ML, Muren E, Gustavsson HO, Josefsson LG, Rask L (1991) Analysis of the promoter region of napin genes from Brassica napus demonstrates binding of nuclear-protein in vitro to a conserved sequence motif. Eur J Biochem 197:741–746PubMedCrossRefGoogle Scholar
  20. Finer JJ, Vain P, Jones MW, McMullen MD (1992) Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep 11:323–328CrossRefGoogle Scholar
  21. Forde BG, Heyworth A, Pywell J, Kreis M (1985). Nucleotide sequence of a B1 hordein gene and the identification of possible upstream regulatory elements in endosperm storage protein genes from barley, wheat and maize. Nucleic Acids Res 13:7327–7339PubMedGoogle Scholar
  22. Frisch DA, van der Geest AHM, Dias K, Hall TC (1995) Chromosomal integration is required for spatial regulation of expression of the β-phaseolin promoter. Plant J 7:503–512CrossRefGoogle Scholar
  23. Fujiwara T, Beachy RN (1994) Tissue-specific and temporal regulation of a β-conglycinin gene: roles of the RY repeat and other cis-acting elements. Plant Mol Biol 24:261–272PubMedCrossRefGoogle Scholar
  24. Fujiwara T, Naito S, Chino M, Nagata T (1991) Electroporated protoplasts express seed specific gene promoters. Plant Cell Rep 9:602–606CrossRefGoogle Scholar
  25. Gleave AP, Mitra DS, Mudge SR, Morris BAM (1999) Selectable marker-free transgenic plants without sexual crossing: transient expression of cre recombinase and use of a conditional lethal dominant gene. Plant Mol Biol 40:223–235PubMedCrossRefGoogle Scholar
  26. Goldberg RB (1986) Regulation of plant gene expression. Philos Trans R Soc B 314:343–353ADSGoogle Scholar
  27. Harada JJ, Barker SJ, Goldberg RB (1989) Soybean β-conglycinin genes are clustered in several DNA regions and are regulated by transcriptional and posttranscriptional processes. Plant Cell 1:415–425PubMedCrossRefGoogle Scholar
  28. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300PubMedCrossRefGoogle Scholar
  29. Holdsworth MJ, Muñoz-Blanco J, Hammond KM, Colot V, Schuch W, Bevan MW (1995) The maize transcription factor Opaque-2 activates a wheat glutenin promoter in plant and yeast cells. Plant Mol Biol 29:711–720PubMedCrossRefGoogle Scholar
  30. Horvath H, Huang JT, Wong O, Kohl E, Okita T, Kannangara CG, von Wettstein D (2000) The production of recombinant proteins in transgenic barley grains. Proc Natl Acad Sci USA 97:1914–1919PubMedCrossRefADSGoogle Scholar
  31. Izawa T, Foster R, Chua NH (1993) Plant bZIP protein DNA binding specificity. J Mol Biol 230:1131–1144PubMedCrossRefGoogle Scholar
  32. Izawa T, Foster R, Nakajima M, Shimamoto K, Chua N-H (1994) The rice bZlP transcriptional activator RlTA-1 is highly expressed during seed development. Plant Cell 6:1277–1287PubMedCrossRefGoogle Scholar
  33. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405Google Scholar
  34. Jordan MC (2003). Green fluorescent protein as a visual marker for wheat transformation. Plant Cell Rep 19:1069–1075CrossRefGoogle Scholar
  35. Kalla R, Shimamoto K, Potter R, Nielsen PS, Linnestad C, Olsen O-A (1994) The promoter of the barley aleurone-specific gene encoding a putative 7 kDa lipid transfer protein confers aleurone cell-specific expression in transgenic rice. Plant J 6:849–860PubMedCrossRefGoogle Scholar
  36. Kawagoe Y, Campbell BR, Murai N (1994) Synergism between CACGTG (G-box) and CACCTG cis-elements is required for activation of the bean seed storage protein β-phaseolin gene. Plant J 5:885–890PubMedCrossRefGoogle Scholar
  37. Kim SY, Chung HJ, Thomas TL (1997) Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11:1237–1251PubMedCrossRefGoogle Scholar
  38. Kluth A, Sprunck S, Becker D, Lörz H, Lütticke S (2002) 5′ deletion of a gbss1 promoter region from wheat leads to changes in tissue and developmental specificities. Plant Mol Biol 49:665–678CrossRefGoogle Scholar
  39. Kreis M, Williamson MS, Forde J, Schmutz D, Clark J, Buxton B, Pywell J, Marris C, Henderson J, Harris N, Shewry PR, Forde BG, Miflin BJ (1986) Differential gene expression in the developing barley endosperm. Philos Trans R Soc B 314:355–365ADSGoogle Scholar
  40. Lessard PA, Allen RD, Bernier F, Crispine JD, Fujiwara T, Beachy RN (1991) Multiple nuclear factors interact with upstream sequences of differentially regulated β-conglycinin genes. Plant Mol Biol 16:397–413PubMedCrossRefGoogle Scholar
  41. Luan S, Bogorad L (1992) A rice cab gene promoter contains separate cis-acting elements that regulate expression in dicot and monocot plants. Plant Cell 4:971–981PubMedCrossRefGoogle Scholar
  42. Marzábal P, Busk PK, Ludevid MD, Torrent M (1998) The bifactorial endosperm box of γ-zein gene: characterisation and function of the Pb3 and GZM cis-acting elements. Plant J 16:41–52PubMedCrossRefGoogle Scholar
  43. Matthews PR, Wang MB, Waterhouse PM, Thornton S, Fieg SJ, Gubler F, Jacobsen JV (2001) Marker gene elimination from transgenic barley, using co-transformation with adjacent ‘twin T-DNAs’ on a standard Agrobacterium transformation vector. Mol Breed 7:195–202CrossRefGoogle Scholar
  44. Mortin RL, Quiggin D (1995) Regulation of seed storage protein gene expression. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, Inc., New York, pp 103–138Google Scholar
  45. Müller M, Knudsen S (1993) The nitrogen response of a barley C-hordein promoter is controlled by positive and negative regulation of the GCN4 and endosperm box. Plant J 4:343–355PubMedzbMATHCrossRefGoogle Scholar
  46. Nagel R, Eliott A, Masel A, Birch RG, Manners JM (1990) Electroporation of binary Ti plasmid vector into Agrobacterium tumefaciens and Agrobacterium rhizogenes. FEMS Microbiol Lett 67:325–328CrossRefGoogle Scholar
  47. Norre F, Peyrot C, Garcia C, Rancé I, Drevet J, Theisen M, Gruber V (2002) Powerful effect of an atypical bifactorial endosperm box from wheat HMWG-Dx5 promoter in maize endosperm. Plant Mol Biol 50:699–712PubMedCrossRefGoogle Scholar
  48. Onate L, Vicente-Carbajosa J, Lara P, Diaz I, Carbonero P (1999) Barley BLZ2, a seed-specific bZIP protein that interacts with BLZ1 in vivo and activates transcription from the GCN4-like motif of B-hordein promoters in barley endosperm. J Biol Chem 274:9175–9182PubMedCrossRefGoogle Scholar
  49. Onodera Y, Suzuki A, Wu CY, Washida H, Takaiwa F (2001) A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. J Biol Chem 276:14139–14152PubMedGoogle Scholar
  50. Patel M, Johnson JS, Brettell RIS, Jacobsen J, Xue G-P (2000) Transgenic barley expressing a fungal xylanase gene in the endosperm of the developing grain. Mol Breed 6:113–124CrossRefGoogle Scholar
  51. Pettersson M, Schaffner W (1987) A purine-rice DNA sequence motif present in SV40 and lymphotropic papovirus binds a lymphoid-specific factor and contributes to enhancer activity in lymphoid cells. Gene Dev 1:962–972Google Scholar
  52. Quayle T, Feix G (1992) Functional analysis of the -300 region of maize genes. Mol Gen Genet 231:369–374PubMedCrossRefGoogle Scholar
  53. Reeves CD, Okita TW (1987) Analyses of α/β-type gliadin genes from diploid and hexaploid wheats. Gene 52:257–266PubMedCrossRefGoogle Scholar
  54. Reidt W, Wohlfarth T, Ellerström M, Czihal A, Tewes A, Ezcurra I, Rask L, Bäumlein H (2000) Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J 21:401–408PubMedCrossRefGoogle Scholar
  55. Remans T, Schenk PM, Manners JM, Grof CPL, Elliott AR (1999) A protocol for the fluorometric quantification of mGFP5-ER and sGFP(S65T) in transgenic plants. Plant Mol Biol Rep 17:385–395CrossRefGoogle Scholar
  56. Ribeiro MD, Kushner P, Baxter MD (1995) The nuclear hormone receptor gene superfamily. Annu Rev Med 46:443–453PubMedCrossRefGoogle Scholar
  57. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, New YorkGoogle Scholar
  58. Schirm S, Jiriciny J, Schaffner W (1987) The SV40 enhancer sequence can be dissected into multiple segments, each with a different cell-type specificity. Gene Dev 1:65–74PubMedGoogle Scholar
  59. Schledzewski K, Mendel RR (1994) Quantitative transient gene expression: comparison of the promoters for maize polyubiquitin1, rice actin1, maize-derived Emu and CaMV 35S in cells of barley, maize and tobacco. Transgenic Res 3:249–255CrossRefGoogle Scholar
  60. Schubert R, Panitz R, Manteuffel R, Nagy I, Wobus U, Bäumlein H (1994) Tissue-specific expression of an oat 12S seed globulin gene in developing tobacco seeds: differential mRNA and protein accumulation. Plant Mol Biol 26:203–210PubMedCrossRefGoogle Scholar
  61. Schünmann PHD, Coia G, Waterhouse PM (2002) Biopharming the SimpliRED(TM) HIV diagnostic reagent in barley, potato and tobacco. Mol Breed 9:113–121CrossRefGoogle Scholar
  62. Seidel HM, Milocco LH, Lamb P, Darnell JE Jr, Stein RB, Rosen J (1995) Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. PNAS 92:3041–3045PubMedCrossRefADSGoogle Scholar
  63. Shewry PR (1995) Cereal seed storage proteins. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, Inc., New York, pp 45–72Google Scholar
  64. Shotwell MA, Boyer SK, Chesnut RS, Larkins BA (1990) Analysis of seed storage protein genes of oats. J Biol Chem 265:9652–9658PubMedGoogle Scholar
  65. 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 33:259–270PubMedCrossRefGoogle Scholar
  66. Stalberg K, Ellerstom M, Ezcurra I, Ablov S, Rask L (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199:515–519PubMedGoogle Scholar
  67. Takaiwa F, Yoshihara T, Washida H, Tanabe F, Ozawa K, Yamanouchi U, Yamada K, Wu C-Y, Toki S (1996) Characterization of common cis-regulatory elements responsible for endosperm-specific expression of rice glutelin gene. Int Rice Res Note 21:17Google Scholar
  68. Tang W, Perry SE (2003) Binding site selection for the plant MADS domain protein AGL15: an in vitro and in vivo study. J Biol Chem 278:28154–28159PubMedCrossRefGoogle Scholar
  69. Thomas MS, Flavell RB (1990) Identification of an enhancer element for the endosperm-specific expression of high molecular weight glutenin. Plant Cell 2:1171–1180PubMedCrossRefGoogle Scholar
  70. Ueda T, Waverczak W, Ward K, Sher N, Ketudat M, Schmidt RJ, Messing J (1992) Mutations of the 22- and 27-kD zein promoters affect transactivation by the opaque−2 protein. Plant Cell 4:701–709PubMedCrossRefGoogle Scholar
  71. Ueda T, Wang Z, Pham N, Messing J (1994) Identification of a transcriptional activator-binding element in the 27-kilodalton zein promoter, the −300 element. Mol Cell Biol 14:4350–4359PubMedGoogle Scholar
  72. Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci USA 94:7685–7690PubMedCrossRefADSGoogle Scholar
  73. Vicente-Carbajosa J, Onate L, Lara P, Diaz I, Carbonero P (1998) Barley BLZ1: a bZIP transcriptional activator that interacts with endosperm-specific gene promoters. Plant J 13:629–640PubMedCrossRefGoogle Scholar
  74. Vickers CE (2004) Functional analysis of the endosperm-specific AsGlo1 promoter. Ph.D. Thesis, The University of Queensland, Brisbane, Queensland, AustraliaGoogle Scholar
  75. Vickers CE, Xue G-P, Gresshoff PM (2003) A synthetic xylanase as a novel reporter in plants. Plant Cell Rep 22:135–140PubMedCrossRefGoogle Scholar
  76. Vinson CR, Hai TW, Boyd SM (1993) Dimerization specificity of the leucine zipper-containing bZIP motif on DNA binding: prediction and rational design. Gene Dev 7:1047–1058PubMedGoogle Scholar
  77. Walling L, Drews GN, Goldberg RB (1986) Transcriptional and post-transcriptional regulation of soybean seed protein mRNA levels. Proc Natl Acad Sci USA 83:2123–2127PubMedCrossRefADSGoogle Scholar
  78. Wan YC, Lemaux PG (1994) Generation of large numbers of independently transformed fertile barley plants. Plant Physiol 104:37–48PubMedGoogle Scholar
  79. Wang Z, Ueda T, Messing J (1998) Characterization of the maize prolamin box-binding factor-1 (PBF-1) and its role in the developmental regulation of the zein multigene family. Gene 223:321–332PubMedCrossRefGoogle Scholar
  80. Wang H, Caruso LV, Downie AB, Perry SE (2004) The embryo MADS domain protein AGAMOUS-like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 16:1206–1219PubMedCrossRefGoogle Scholar
  81. Washida H, Wu C-Y, Suzuki A, Yamanouchi U, Akihama T, Harada K, Takaiwa F (1999) Identification of cis-regulatory elements required for endosperm expression of the rice storage protein glutelin gene GluB-1. Plant Mol Biol 40:1–12PubMedCrossRefGoogle Scholar
  82. Wirtzens B, Brettell RIS, Murray FR, McElroy D, Li Z, Dennis ES (1998) Comparison of three selectable marker genes for transformation of wheat by microprojectile bombardment. Aust J Plant Physiol 25:39–44CrossRefGoogle Scholar
  83. Wu C-Y, Suzuki A, Washida H, Takaiwa F (1998) The GCN4 motif in a rice glutelin gene is essential for endosperm-specific gene expression and is activated by Opaque-2 in transgenic rice plants. Plant J 14:673–683PubMedCrossRefGoogle Scholar
  84. Wu C-Y, Washida H, Onodera Y, Harada K, Takaiwa F (2000) Quantitative nature of the Prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. Plant J 23:415–421PubMedCrossRefGoogle Scholar
  85. Xue GP (2005) A CELD-fusion method for rapid determination of the DNA-binding sequence specificity of novel plant DNA-binding proteins. Plant J 41:638–649PubMedCrossRefGoogle Scholar
  86. Xue G-P, Loveridge CW (2004) HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37:326–339PubMedCrossRefGoogle Scholar
  87. Xue G-P, Patel M, Johnson JS, Smythe DJ, Vickers CE (2003) Selectable marker-free transgenic barley producing a high level of cellulase (1,4-β-glucanase) in developing grains. Plant Cell Rep 21:1088–1094PubMedCrossRefGoogle Scholar
  88. Xue G-P, Bower NI, McIntyre CL, Riding GA, Kazan K, Shorter R (2006) TaNAC69 from the NAC superfamily of transcription factors is up-regulated by abiotic stresses in wheat and recognises two consensus DNA-binding sequences. Funct Plant Biol 33:43–57CrossRefGoogle Scholar
  89. Yoshino M, Kanazawa A, Tsutsumi K, Nakamura I, Shimamoto Y (2001) Structure and characterization of the gene encoding a subunit of soybean ß-conglycinin. Genes Genet Syst 76:99–105PubMedCrossRefGoogle Scholar
  90. Zakharov A, Giersberg M, Hosein F, Melzer M, Muntz K, Saalbach I (2004) Seed-specific promoters direct gene expression in non-seed tissue. J Exp Bot 55:1463–1471PubMedCrossRefGoogle Scholar
  91. Zhang Y, Darlington H, Jones HD, Halford NG, Napier JA, Davey MR, Lazzeri PA, Shewry PR (2003) Expression of the gamma-zein protein of maize in seeds of transgenic barley: effects on grain composition and properties. Theor Appl Genet 106:1139–1146PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Claudia E. Vickers
    • 1
    • 2
    • 3
    Email author
  • Gangping Xue
    • 1
  • Peter M. Gresshoff
    • 2
  1. 1.CSIRO Plant IndustrySt Lucia, BrisbaneAustralia
  2. 2.ARC Centre of Excellence for Integrative Legume ResearchThe University of QueenslandSt LuciaAustralia
  3. 3.Department of Biological SciencesThe University of EssexColchesterUK

Personalised recommendations