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ZmGrp3: identification of a novel marker for root initiation in maize and development of a robust assay to quantify allele-specific contribution to gene expression in hybrids

Theoretical and Applied Genetics volume 113, pages 1305–1315 (2006)Cite this article

Abstract

This study comprises a comprehensive gene expression analysis of the root tip specific maize gene ZmGrp3. In the first part of this paper expression of ZmGrp3 was studied in maize inbred lines. First, RNA in situ hybridization experiments confined the expression of ZmGrp3 to the columella and the epidermis of all embryonic and postembryonic root types. Second, Northern-blot analyses of the maize root initiation mutants rtcs and lrt1 revealed that the ZmGrp3 gene is not expressed prior to root initiation, thus providing a novel marker for this developmental process. Finally, a comprehensive expression profiling in 42 tissues via the Lynx MPSS system revealed almost exclusive expression of ZmGrp3 in maize roots. In the second part of this survey, ZmGrp3 expression was assayed in maize hybrids. In this context, a novel approach to quantify allele-specific contribution to gene expression in maize hybrids was developed. This assay combines RT–PCR amplification of polymorphisms between two alleles and subsequent quantification of allele-specific gene expression via a combination of didesoxyterminator assays and capillary electrophoresis. Allelic expression of the ZmGrp3 gene in six reciprocal hybrids generated from three ZmGrp3 alleles was analyzed via a new statistical mixed model approach.

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References

  • Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. Plant Cell 15:2236–2239

    PubMed  CAS  Article  Google Scholar 

  • Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH et al. (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18:630–634

    PubMed  CAS  Article  Google Scholar 

  • Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111

    PubMed  CAS  Article  Google Scholar 

  • Christensen TM, Veijlupkova Z, Sharma YK, Arthur KM, Spatafora JW et al (2003) Conserved subgroups and developmental regulation in the monocot rop gene family. Plant Physiol 133:1791–1808

    PubMed  CAS  Article  Google Scholar 

  • Connolly J, Wachendorf M (2001) Developing multisite dynamic models of mixed species plant communities. Ann Bot 88:703–712

    Article  Google Scholar 

  • Goddemeier ML, Wulff D, Feix G (1998) Root-specific expression of a Zea mays gene encoding a novel glycine-rich protein, grp3. Plant Mol Biol 36:799–802

    PubMed  CAS  Article  Google Scholar 

  • Guo M, Rupe M, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16:1707–1716

    PubMed  CAS  Article  Google Scholar 

  • Hetz W, Hochholdinger F, Schwall M, Feix G (1996) Isolation and characterisation of rtcs a mutant deficient in the formation of nodal roots. Plant J 10:845–857

    CAS  Article  Google Scholar 

  • Hochholdinger F, Feix G (1998a) Early post-embryonic root formation is specifically affected in the maize mutant lrt1. Plant J 16:247–255

    Article  Google Scholar 

  • Hochholdinger F, Feix G (1998b) Cyclin expression is completely suppressed at the site of crown root formation in the nodal region of the maize root mutant rtcs. J Plant Physiol 153:425–429

    CAS  Google Scholar 

  • Hochholdinger F, Wulff D, Reuter K, Park WJ, Feix G (2000) Tissue specific expression of AUX1 in maize roots. J Plant Physiol 157:315–319

    CAS  Google Scholar 

  • Hochholdinger F, Park WJ, Feix G (2001) Cooperative action of SLR1 and SLR2 is required for lateral root-specific cell-elongation in maize. Plant Physiol 125:1529–1539

    PubMed  CAS  Article  Google Scholar 

  • Hochholdinger F, Park WJ, Sauer M, Woll K (2004a) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci 9:42–48

    CAS  Article  Google Scholar 

  • Hochholdinger F, Woll K, Sauer M Dembinsky D (2004b) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programs. Ann Bot 93:359–368

    CAS  Article  Google Scholar 

  • Hochholdinger F, Guo L, Schnable PS (2004c) Lateral roots affect the proteome of the primary root of maize (Zea mays L.). Plant Mol Biol 56:397–412

    CAS  Article  Google Scholar 

  • Hochholdinger F, Woll K, Sauer M, Feix G (2005a) Functional genomic tools in support of the genetic analysis of root development in maize (Zea mays L.). 50th anniversary edition of Maydica (in press)

  • Hochholdinger F, Woll K, Guo L, Schnable PS (2005b) Analysis of the soluble proteome of maize (Zea mays L.) primary roots reveals drastic changes in protein composition during early development. Proteomics 18:4885–4893

    Article  Google Scholar 

  • Hoecker N, Keller B, Piepho H-P, Hochholdinger F (2006) Manifestation of heterosis during early maize (Zea mays L.) root development. Theor Appl Genet 112:421–429

    PubMed  Article  Google Scholar 

  • Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997

    PubMed  CAS  Article  Google Scholar 

  • Kynast RG, Riera-Lizarazu O, Vales MI, Okagaki RJ, Maquieira SB et al (2001) A complete set of maize individual chromosome additions to the oat genome. Plant Physiol 125:1216–1227

    PubMed  CAS  Article  Google Scholar 

  • Lim J, Helariutta Y, Specht CD, Jung J, Sims L et al (2000) Molecular analysis of the SCARECROW gene in maize reveals a common basis for radial patterning in diverse meristems. Plant Cell 12:1307–1318

    PubMed  CAS  Article  Google Scholar 

  • Matsuyama T, Satoh H, Yamada Y, Hashimoto T (1999) A maize glycine-rich protein is synthesized in the lateral root cap and accumulates in the mucilage. Plant Physiol 120:665–674

    PubMed  CAS  Article  Google Scholar 

  • Ponce G, Lujan R, Campos WE, Reyes A, Nieto-Sotelo J et al (2000) Three maize root-specific genes are not correctly expressed in regenerated caps in the absence of the quiescent center. Planta 211:23–33

    PubMed  CAS  Article  Google Scholar 

  • Poroyko V, Hejlek LG, Spollen WG, Springer GK, Nguyen HT et al (2005) The maize root transcriptome by serial analysis of gene expression. Plant Physiol 138:1700–1710

    PubMed  CAS  Article  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    PubMed  CAS  Article  Google Scholar 

  • Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304

    PubMed  CAS  Article  Google Scholar 

  • Sauer M, Jakob A, Nordheim A, Hochholdinger F (2006) Proteomic analysis of shoot-borne root initiation in maize (Zea mays L.). Proteomics 6:2530–2541

    PubMed  CAS  Article  Google Scholar 

  • Wen TJ, Schnable PS (1994) Analyses of mutants of three genes that influence root hair development in Zea mays (Gramineae) suggest that root hairs are dispensable. Am J Bot 81:833–842

    Article  Google Scholar 

  • Wen TJ, Hochholdinger F, Sauer M, Bruce W, Schnable PS (2005) The roothairless1 gene of maize (Zea mays) encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol 138:1637–1643

    PubMed  CAS  Article  Google Scholar 

  • Woll K, Borsuk L, Stransky H, Nettleton D, Schnable PS, Hochholdinger F (2005) Isolation, characterization and pericycle specific transcriptome analyses of the novel maize (Zea mays L.) lateral and seminal root initiation mutant rum1. Plant Physiol 139:1255–1267

    PubMed  CAS  Article  Google Scholar 

  • Zimmermann R, Werr W (2005) Pattern formation in the monocot embryo as revealed by NAM and CUC3 orthologues from Zea mays L. Plant Mol Biol 58:669–685

    PubMed  CAS  Article  Google Scholar 

Download references

Acknowledgment

We thank Dr. Ron Phillips (University of Minnesota) for the gift of genomic DNA of oat–maize addition lines. Work on this project in F.H.’s and H.-P.P.’s laboratories was supported by the Deutsche Forschungsgemeinschaft (DFG) framework program SPP1149 “heterosis in plants”. Root research in F.H.’s laboratory is supported by the DFG grant HO2249/4, and the project B16 of the Sonderforschungsbereich 446 “cell behavior in eukaryotes”.

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Authors and Affiliations

  1. Center for Plant Molecular Biology (ZMBP), Department of General Genetics, Eberhard-Karls-University Tuebingen, Auf der Morgenstelle 28, Tuebingen, 72076, Germany

    Katrin Woll, Angela Dressel & Frank Hochholdinger

  2. DuPont Crop Genetics Research, Wilmington, DE, 19880-353, USA

    Hajime Sakai

  3. Bioinformatics Unit, Institution for Crop Production and Grassland Research, University of Hohenheim, Stuttgart, 70599, Germany

    Hans-Peter Piepho

Authors
  1. Katrin Woll
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  2. Angela Dressel
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  3. Hajime Sakai
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  4. Hans-Peter Piepho
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  5. Frank Hochholdinger
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Corresponding author

Correspondence to Frank Hochholdinger.

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Communicated by E: Guiderdoni

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Woll, K., Dressel, A., Sakai, H. et al. ZmGrp3: identification of a novel marker for root initiation in maize and development of a robust assay to quantify allele-specific contribution to gene expression in hybrids. Theor Appl Genet 113, 1305–1315 (2006). https://doi.org/10.1007/s00122-006-0384-1

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  • DOI: https://doi.org/10.1007/s00122-006-0384-1

Genbank Accessions of ZmGrp3 alleles

  • Allele UH002: DQ267623
  • Allele UH250: DQ267624
  • Allele UH301: DQ267625