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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Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. Plant Cell 15:2236–2239
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
Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111
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
Connolly J, Wachendorf M (2001) Developing multisite dynamic models of mixed species plant communities. Ann Bot 88:703–712
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
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
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
Hochholdinger F, Feix G (1998a) Early post-embryonic root formation is specifically affected in the maize mutant lrt1. Plant J 16:247–255
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
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
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
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
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
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
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
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
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997
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
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
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
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
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
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
Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304
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
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
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
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
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
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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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