Skip to main content
SpringerLink
Log in

Cellular localization of the embryo-specific Hybrid PRP from Zea mays, and characterization of promoter regulatory elements of its gene

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The expression, regulation and cellular localization of ZmHyPRP, a gene marker of embryo differentiation whose expression declines after ABA induction, was studied. ZmHyPRP is a proline-rich protein with a C-terminal domain having eight cysteines in a CM8 pattern. Transient expression in onion epidermal cells, transformed with a 2x35S::ZmHyPRP-GFP construction, indicated the protein is present in vesicles lining the membrane of the cell. The ZmHyPRP gene expression is under the control of classic promoter seed-specific regulatory elements such as Sph/RY and G-boxes, suggesting regulation by B3 and b-ZIP transcription factors. Promoter deletion analysis, by particle-bombardment transient transformation of maize immature embryos with serial deletions of the promoter fused to GUS, showed the presence of two negative regulatory elements, NE1 (−2070 to −1280) and NE2 (−232 to −178), in the ZmHyPRP promoter. By selective deletion or mutation of ZmHyPRP regulatory promoter elements we conclude that the promoter expression is attenuated by the NE2 element as well as by the G-box2 and the Sph1-2 box together with the G-box2.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14:1391–1403

    Article  CAS  PubMed  Google Scholar 

  • Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13:624–630

    Article  CAS  PubMed  Google Scholar 

  • Busk PK, Pagés M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    Article  CAS  PubMed  Google Scholar 

  • Cavener DR, Ray SC (1991) Eukaryotic start and stop translation sites. Nucleic Acids Res 19:3185–3192

    Article  CAS  PubMed  Google Scholar 

  • Chern M-S, Bobb AJ, Bustos MM (1996a) The regulator of MAT2 (ROM2) protein binds to early maturation promoters and represses PvALF-activated transcription. Plant Cell 8:305–321

    CAS  PubMed  Google Scholar 

  • Chern M-S, Eiben HG, Bustos MM (1996b) The developmentally regulated bZip factor ROM1 modulates transcription from lectin and storage protein genes in bean embryos. Plant J 10:135–148

    Article  CAS  PubMed  Google Scholar 

  • Dickinson CD, Evans RP, Nielsen NC (1988) RY repeats are conserved in the 5′-flanking regions of legume seed protein gene. Nucleic Acids Res 16:371

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    CAS  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(suppl):S15–S45.

    Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi TS, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  CAS  PubMed  Google Scholar 

  • Hattori T, Vasil V, Rosenkrans L, Hannah LC, McCarty DR, Vasil IK (1992) The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev 6:609–618

    Article  CAS  PubMed  Google Scholar 

  • Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51–59

    Article  CAS  PubMed  Google Scholar 

  • Hong B, Barg R, Ho TD (1992) Developmental and organ-specific expression of an ABA- and stress-induced protein in barley. Plant Mol Biol 18:663–674

    Article  CAS  PubMed  Google Scholar 

  • Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  PubMed  Google Scholar 

  • Jones RJ, Brenner ML (1987) Distribution of abscisic acid in maize kernel during grain filling. Plant Physiol 83:905–909

    Article  CAS  PubMed  Google Scholar 

  • Jose M, Puigdomènech P (1993) Structure and expression of genes coding for structural proteins of the plant cell wall. New Phytol. 125:259–282 Tansley Review No 55

    Article  CAS  Google Scholar 

  • Jose-Estanyol M, Puigdomènech P (1998) Developmental and hormonal regulation of genes coding for proline-rich proteins in female inflorescences and kernels of maize. Plant Physiol 116:485–494

    Article  CAS  PubMed  Google Scholar 

  • Jose-Estanyol M, Ruiz-Avila L, Puigdomènech P (1992) A maize embryo-specific gene encodes a proline-rich and hydrophobic protein. Plant Cell 4:413–423

    CAS  PubMed  Google Scholar 

  • Jose-Estanyol M, Gomis-Rüth FX, Puigdomènech P (2004) The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiol Biochem 42:355–365

    Article  CAS  PubMed  Google Scholar 

  • Jose-Estanyol M, Pérez P, Puigdomènech P (2005) Expression of the promoter of HyPRP, an embryo-specific gene from Zea mays in maize and tobacco transgenic plants. Gene 356:146–152

    Article  CAS  PubMed  Google Scholar 

  • Kieliszewvski MJ (2001) The latest hype on Hyp-O-glycosylation codes. Phytochemistry 57:319–323

    Article  Google Scholar 

  • Kieliszewvski MJ, Lamport DTA (1994) Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J 5:157–172

    Article  Google Scholar 

  • Kroj T, Savino G, Valon Ch, Giraudat J, Parcy F (2003) Regulation of storage protein gene expression in Arabidopsis. Development 130:6065–6073

    Article  CAS  PubMed  Google Scholar 

  • Li G, Bishop KJ, Chandrasekharan MB, Hall TC (1999) beta-Phaseolin gene activation is a two-step process: PvALF facilitated chromatin modification followed by abscisic acid-mediated gene activation. Proc Natl Acad Sci USA 96:7104–7109

    Article  CAS  PubMed  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  CAS  PubMed  Google Scholar 

  • Luerßen H, Kirik V, Hermann P, Miséra S (1998) FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764

    Article  PubMed  Google Scholar 

  • Marcotte WR Jr, Rusell SH, Quatrano RS (1989) Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1:969–976

    CAS  PubMed  Google Scholar 

  • McCarty DR, Hattori T, Carson ChB, Vasil V, Lazar M, Vasil IK (1991) The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66:895–905

    Article  CAS  PubMed  Google Scholar 

  • McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2:163–171

    CAS  PubMed  Google Scholar 

  • Mundy J, Yamaguchi-Shinozaki K, Chua N-H (1990) Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc Natl Acad Sci USA 87:1406–1410

    Article  CAS  PubMed  Google Scholar 

  • Nantel A, Quatrano RS (1996) Characterization of three rice basic/leucine zipper factors including two inhibitors of EmBP-1 DNA binding activity. J Biol Chem 271:31296–31305

    Article  CAS  PubMed  Google Scholar 

  • Neil SJ, Horgan R, Parry AD (1986) The carotenoid and abscisic acid content of viviparous kernels and seedlings of Zea mays L. Planta 169:87–96

    Article  Google Scholar 

  • North H, Baud S, Debeaujon I, Dubos Ch, Dubreucq B, Grappin P, Jullien M, Lepinec L, Marion-Poll A, Miquel M, Rajjou L, Routaboul J-M, Caboche M (2010) Arabidopsis seed secrets unraveled after a decade of genetic and genomics-driven research. Plant J 61:971–981

    Article  CAS  PubMed  Google Scholar 

  • Panitz R, Borisjuk L, Manteuffel R, Wobus U (1995) Transient expression of storage-protein genes during early embryogenesis of Vicia faba synthesis and metabolization of vicilin and legumin in the embryo, suspensor and endosperm. Planta 196:765–774

    Article  CAS  Google Scholar 

  • Rohde A, Kurup S, Holdsworth M (2000) ABI3 emerges from the seed. Trends Plant Sci 5:418–419

    Article  CAS  PubMed  Google Scholar 

  • Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepinec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54:608–620

    Article  CAS  PubMed  Google Scholar 

  • Scott A, Wyatt S, Tson PL, Robertson D, Strömgren A (1999) Model system for plant cell biology: GFP imaging in living onion epidermal cells. BioTechniques 26:1127–1132

    Google Scholar 

  • Shen Q, Zhang P, Ho T-HD (1996) Modular nature of abscisic acid (ABA) response complexes. Composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8:1107–1119

    CAS  PubMed  Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fisher RL, Goldberg RB, Harada JJ (2001) Leafy cotyledon2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M, McCarty DR (2008) Functional symmetry of the B3 network controlling seed development. Curr Opin Plant Biol 11:548–553

    Article  CAS  PubMed  Google Scholar 

  • Thomas TL (1993) Gene expression during plant embryogenesis and germination: an overview. Plant Cell 5:1401–1410

    CAS  PubMed  Google Scholar 

  • Vasil V, Jr Marcotte, Rosenkrans L, Cocciolone SM, Vasil IK, Quatrano RS, McCarty DR (1995) Overlap of Viviparous1 (VP1) and abscisic acid response elements in the Em promoter: G-box elements are sufficient but not necessary for VP1 transactivation. Plant Cell 7:1511–1518

    CAS  PubMed  Google Scholar 

  • Weber H, Borisjuk L, Wobus U (2005) Molecular physiology of legume seed development. Ann Rev Plant Biol 56:253–279

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are indebted to D. Ludevid (CRAG) for critical interpretation of the protein expression results, and to M. Amoros for assistance in confocal microscopy and P. Fontanet for help in the greenhouse. This work was supported by grants BI02004-01577, BI02007-64791. Consolider CSD2007-00036 Centro de Agrigenómica y Orientación Alimentaria (MICINN). SGR2009 703 Grup de Recerca Consolidat “Genetica Molecular Vegetal” (AGAUR). Xarxa de referencia en Biotecnologia (DIUE).

Author information

Authors and Affiliations

  1. Centre de Recerca en Agrigenòmica (CRAG), CSIC-IRTA-UAB-UB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 081993, Barcelona, Spain

    M. Jose-Estanyol & P. Puigdomènech

Authors
  1. M. Jose-Estanyol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Puigdomènech
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Jose-Estanyol.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11103_2012_9951_MOESM1_ESM.docx

Supplementary material 1 (DOCX 16 kb): Description of primers used to obtain the constructions used in the ZmHyPRP promoter study by transient expression

11103_2012_9951_MOESM2_ESM.ppt

Supplementary material 2 (PPT 481 kb): Comparative gel blot analysis of the mRNA expression pattern of various genes during maize W64A embryogenesis. a Each of the indicated cDNA probes was hybridized to total RNA isolated from W64A wild-type embryos harvested at different days after anthesis (10 μg RNA/slot). b Control of grain and embryo fresh weights at different days after anthesis. (Ι) Standard deviation

11103_2012_9951_MOESM3_ESM.pptx

Supplementary material 3 (PPTX 718 kb): Bombardment control studies. Comparative mRNA gel blot analysis from maize excised embryos (16–18 dap), incubated for different times in MSO: 1- zero; 2- 24 h; 3- 48 h. (10 μg RNA/slot). The same blot was hybridized successively with all the probes. Equal loading was verified by EtBr staining

11103_2012_9951_MOESM4_ESM.pptx

Supplementary material 4 (PPTX 4180 kb): Comparative gel blot analysis of the mRNA expression pattern of genes during maize vp1 embryogenesis from semi-dormant embryos. Each of the indicated cDNA probes was hybridized to total RNA isolated from vp1 semi-dormant embryos harvested at different days after anthesis. Equal input was verified by EtBr staining. The same blot was successively hybridized with all the probes. 10 μg RNA/slot

11103_2012_9951_MOESM5_ESM.pptx

Supplementary material 5 (PPTX 70 kb): Distribution of Sph/RY, G-boxes and TATAAA box elements in plant gene promoters. Nucleotide distances from the ATG are indicated.▲ b-Zip G-boxes; △ b-Zip opaque- boxes; ◆ Sph/RY elements; ▮ TATAAA box. Gene references: At2S3 Z24744; BnnapA FN807060; PvPHSβ J01263; PvDLEC2 K03289; VfLeB4 X03677; Hvβ-Hor2 X87232; ZmRAB17 X15994; TaEm X52103; OsRAB16a Y00842 and ZmC1 X06333

11103_2012_9951_MOESM6_ESM.xlsx

Supplementary material 6 (XLSX 20 kb): Presence of Sph/RY elements in different plant gene promoters. Consensus sequences for the Sph1 restriction site, Sph and RY elements are in bold. Sequences around the central double repeat consensus sequence are shown. Nucleotides divergent from consensus sequences are in lower case. Described genes are as follows: ZmHyPRP (X60432); ZmC1 X06333; ZmRAB17 X15994; TaEm X52103; Osem U22102; OsRAB16a Y00842; Hvβ-Hor2 X87232; PvDLEC2 K03289; VfLeB4 X03677; GmG1 X15121; BnnapA FN807060; At2S3 Z24744; AtSDH2-3 At5g65165; AtGA3ox2 At1g80340, PvPHSβ J01263 and PspSI X66368. Sequence position from the ATG is indicated on the left and by a vertical arrow

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jose-Estanyol, M., Puigdomènech, P. Cellular localization of the embryo-specific Hybrid PRP from Zea mays, and characterization of promoter regulatory elements of its gene. Plant Mol Biol 80, 325–335 (2012). https://doi.org/10.1007/s11103-012-9951-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-012-9951-9

Keywords

Search

Navigation