Skip to main content
SpringerLink
Log in

Transcriptional activation of the maize endosperm transfer cell-specific gene BETL1 by ZmMRP-1 is enhanced by two C2H2 zinc finger-containing proteins

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

ZmMRP-1 is a single MYB-domain transcription factor specifically expressed in the transfer cell layer of the maize endosperm, where it directly regulates the expression of a number of transfer cell specific genes and very likely contributes to the regulation of the transfer cell differentiation process. It is still a matter of debate, however, how this type of transcription factors interact with the promoter sequences they regulate. In this work we have investigated the existence of proteins interacting with ZmMRP-1 in the transfer cell nuclei. In a yeast double-hybrid screen we identified two related maize proteins, ZmMRPI-1 and ZmMRPI-2 belonging to the C2H2 zinc finger protein family, which interact with ZmMRP-1 and modulate its activity on transfer cell specific promoters. Two ZmMRPI orthologous genes were also identified in the rice and Arabidopsis genomes. The expression pattern in maize and Arabidopsis suggest a role for these proteins in gene regulation at the exchange surfaces where ZmMRP-1 is expressed providing the first indication of their function. We show that this previously uncharacterized family of proteins encodes nuclear proteins that interact with MYB-related transcription factors through their C-terminal conserved domain.

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

Abbreviations

ANOVA:

Analysis of variance

DAP:

Days after pollination

DMSO:

Dimethyl sulfoxide

EMSA:

Electrophoretic mobility shift assay

GFP:

Green fluorescent protein

GUS:

Beta-glucuronidase

mCherry:

mCherry fluorescent protein

MS:

Murashige and Skoog

PEG:

Polyethylene glycol

ZmMRP-1:

Zea mays MYB-related protein 1

ZmMRPI-1:

ZmMRP-1 interactor-1

ZmMRPI-2:

ZmMRP-1 interactor-2

References

  • Agarwal P, Arora R, Ray S, Singh AK, Singh VP, Takatsuji H, Kapoor S, Tyagi AK (2007) Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Mol Biol 65:467–485

    Article  PubMed  CAS  Google Scholar 

  • Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13:99–102

    Article  PubMed  CAS  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Baranowskij N, Frohberg C, Prat S, Willmitzer L (1994) A novel DNA binding protein with homology to MYB oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J 13:5383–5392

    PubMed  CAS  Google Scholar 

  • Barrero C, Muñiz LM, Gómez E, Hueros G, Royo J (2006) Molecular dissection of the interaction between the transcriptional activator ZmMRP-1 and the promoter of BETL-1. Plant Mol Biol 62:655–668

    Article  PubMed  CAS  Google Scholar 

  • Barrero C, Royo J, Grijota MC, Faye C, Wyatt P, Sanz S, Steinbiss HH, Hueros G (2009) The promoter of ZmMRP-1, a maize transfer cell-specific transcriptional activator, is induced at solute exchange surfaces and responds to transport demands. Planta 229:235–247

    Article  PubMed  CAS  Google Scholar 

  • Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci III 316:1194–1199

    CAS  Google Scholar 

  • Bianchi A, Smith S, Chong L, Elias P, de Lange T (1997) TRF1 is a dimer and bends telomeric DNA. EMBO J 16:1785–1794

    Article  PubMed  CAS  Google Scholar 

  • Birve A, Sengupta AK, Beuchle D, Larsson J, Kennison JA, Rasmuson-Lestander A, Müller J (2001) Su(z)12, a novel Drosophila polycomb group gene that is conserved in vertebrates and plants. Development 128:3371–3379

    PubMed  CAS  Google Scholar 

  • Bouchez D, Camilleri C, Caboche M (1993) A binary vector based on Basta resistance for in planta transformation of Arabidopsis thaliana. C R Acad Sci III 316:1188–1193

    CAS  Google Scholar 

  • Chevray PM, Nathans D (1992) Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc Natl Acad Sci USA 89:5789–5793

    Article  PubMed  CAS  Google Scholar 

  • Churin Y, Adam E, Kozma-Bognar L, Nagy F, Börner T (2003) Characterization of two Myb-like transcription factors binding to CAB promoters in wheat and barley. Plant Mol Biol 52:447–462

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Coe EH, Schaeffer ML (2005) Genetic, physical, maps and database resources for maize. Maydica 50:285–303

    Google Scholar 

  • Davis RW, Smith JD, Cobb BG (1990) A light and electron microscope investigation of the transfer cell region of maize caryopses. Can J Bot 68:471–479

    Article  Google Scholar 

  • Englbrecht CC, Schoof H, Böhm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39–55

    Article  PubMed  Google Scholar 

  • Gamsjaeger R, Liew CK, Loughlin FE, Crossley M, Mackay JP (2007) Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci 32:63–70

    Article  PubMed  CAS  Google Scholar 

  • Gómez E, Royo J, Guo R, Thompson R, Hueros G (2002) Establishment of cereal endosperm expression domains: identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell 14:599–610

    Article  PubMed  Google Scholar 

  • Grotewold E, Sainz MB, Tagliani L, Hernandez JM, Bowen B, Chandler VL (2000) Identification of the residues in the Myb domain of maize C1 that specify the interaction with the bHLHL cofactor R. Proc Natl Acad Sci USA 97:13579–13584

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez-Marcos JF, Costa L, Biderre-Petit C, Khbaya B, O’Sullivan D, Wornmald M, Perez P, Dickinson H (2004) maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16:1288–1301

    Article  PubMed  CAS  Google Scholar 

  • Hill J, Donald KAG, Griffiths DE (1991) DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res 19:5791

    Article  PubMed  CAS  Google Scholar 

  • Hueros G, Varotto S, Salamini F, Thompson RD (1995) Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7:747–757

    Article  PubMed  CAS  Google Scholar 

  • Hueros G, Gómez E, Cheikh N, Edwards F, Weldon M, Salamini F, Thompson RD (1999a) Identification of a promoter sequence from the BETL1 gene cluster able to confer transfer cell-specific expression in transgenic maize. Plant Physiol 121:1143–1152

    Article  PubMed  CAS  Google Scholar 

  • Hueros G, Royo J, Maitz M, Salamini F, Thompson RD (1999b) Evidence for factors regulating transfer cell-specific expression in maize endosperm. Plant Mol Biol 41:403–414

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanag TA, Bevan M (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41:577–585

    Article  PubMed  CAS  Google Scholar 

  • 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 11:1237–1251

    Article  PubMed  CAS  Google Scholar 

  • Krishna SS, Majumdar I, Grishin NV (2003) Structural classification of zinc fingers. Nucleic Acids Res 31:532–550

    Article  PubMed  CAS  Google Scholar 

  • Lara P, Oñate-Sánchez L, Abraham Z, Ferrándiz C, Díaz I, Carbonero P, Vicente-Carbajosa JV (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem 278:21003–21011

    Article  PubMed  CAS  Google Scholar 

  • Locatelli F, Bracales M, Magaraggia F, Faoro F, Manzocchi LA, Coraggio I (2000) The product of the rice myb7 unspliced mRNA dimerizes with the maize leucine zipper Opaque2 and stimulates its activity in a transient expression assay. J Biol Chem 275:17619–17625

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Ho TH, Ho SL, Yu SM (2002) Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of alpha-amylase gene expression. Plant Cell 14:1963–1980

    Article  PubMed  CAS  Google Scholar 

  • Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, Chaudhury AM (1999) Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:296–301

    Article  PubMed  CAS  Google Scholar 

  • Miller JH (1992) A short course in bacterial genetics. A laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Morohashi K, Zhao M, Yang M, Read B, Lloyd A, Lamb R, Grotewold E (2007) Participation of the Arabidopsis bHLH factor GL3 in trichome initiation regulatory events. Plant Physiol 145:736–746

    Article  PubMed  CAS  Google Scholar 

  • Muñiz LM, Royo J, Gómez E, Barrero C, Bergareche D, Hueros G (2006) The maize transfer cell-specific type-A response regulator ZmTCRR-1 appears to be involved in intercellular signalling. Plant J 48:17–27

    Article  PubMed  Google Scholar 

  • Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    Article  PubMed  CAS  Google Scholar 

  • Olsen O, Linnestad C, Nichols S (1999) Developmental biology of the cereal endosperm. Trends Plant Sci 4:253–257

    Article  PubMed  Google Scholar 

  • Phelps-Durr TL, Thomas J, Vahab P, Timmermans MCP (2005) Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17:2886–2898

    Article  PubMed  CAS  Google Scholar 

  • Prigge MJ, Wagner DR (2001) The Arabidopsis SERRATE gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13:1263–1279

    Article  PubMed  CAS  Google Scholar 

  • Raizada MN, Guo-Ling N, Walbot V (2001) Somatic and germinal mobility of the RescueMu transposon in transgenic maize. Plant Cell 13:1587–1608

    Article  PubMed  CAS  Google Scholar 

  • Ramsay NA, Glover BJ (2005) MYB–bHLH–WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10:63–70

    Article  PubMed  CAS  Google Scholar 

  • Royo J, Gómez E, Hueros G (2007) Transfer cells. In: Olsen O-A (ed) Endosperm-development and molecular biology. Plant Cell Monographs Series. Springer, Berlin, pp 73–89

    Google Scholar 

  • Rubio-Somoza I, Martínez M, Díaz I, Carbonero P (2006) HvMCB1, a R1MYB transcription factor from barley with antagonistic regulatory functions during seed development and germination. Plant J 45:17–30

    Article  PubMed  CAS  Google Scholar 

  • Thompson RD, Hueros G, Becker H, Maitz M (2001) Development and functions of seed transfer cells. Plant Sci 160:775–783

    Article  PubMed  CAS  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2(8):e718. doi:10.1371/journal.pone.0000718

    Article  PubMed  Google Scholar 

  • Yang L, Liu Z, Lu F, Dong A, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47:841–850

    Article  PubMed  CAS  Google Scholar 

  • Yu EY, Kim SE, Kim JH, Ko JH, Cho MH, Chung IK (2000) Sequence-specific DNA recognition by the Myb-like domain of plant telomeric protein RTBP1. J Biol Chem 275:24208–24214

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. R.D. Thompson (INRA Unité Mixte de Recherches en Génétique et Ecophysiologie des légumineuses à graines, Dijon, France) for his generous donation of a cDNA library. This work was supported by Spanish Ministerio de Educación y Ciencia (BIO2003-03721 and BIO2006-14190 to G. Hueros).

Author information

Authors and Affiliations

  1. Dpto. Biología Celular y Genética, Universidad de Alcalá, Campus Universitario, Alcalá de Henares, 28870, Madrid, Spain

    Joaquín Royo, Elisa Gómez, Cristina Barrero, Luis Miguel Muñiz, Yolanda Sanz & Gregorio Hueros

Authors
  1. Joaquín Royo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisa Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristina Barrero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luis Miguel Muñiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yolanda Sanz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gregorio Hueros
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregorio Hueros.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 91 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Royo, J., Gómez, E., Barrero, C. et al. Transcriptional activation of the maize endosperm transfer cell-specific gene BETL1 by ZmMRP-1 is enhanced by two C2H2 zinc finger-containing proteins. Planta 230, 807–818 (2009). https://doi.org/10.1007/s00425-009-0987-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-0987-2

Keywords

Search

Navigation