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Grain development and endoreduplication in maize and the impact of heat stress

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Abstract

The post-anthesis development of growing maize kernels is strongly affected by heat stress. The maize cultivar “Spezi” was used to quantify this effect in kernels from 14 days after flowering until maturity. Day/night temperature of control plants was 25/20°C. Stress of 40/25°C was given for seven days or continuously up to maturity. Kernels were analysed weekly for dry matter and extractable DNA. In addition the ploidy levels and the DNA content in intact cell nuclei were determined by flow cytometry. The dry matter reduction started immediately after heat treatment and reached, at maturity, 40% for temporary heat stress and 60% for permanent heat stress. The reduction of extractable DNA started later and was not as extensive. Endopolyploidy was found in all kernel tissues, namely embryo, endosperm and pericarp. In endosperm, 3C nuclei reached their maximum number at approximately 14–17 days, and cells with higher ploidy levels between 21 and 26 days after flowering. Later on 6C nuclei were dominant. The DNA content in intact cells of the endosperm reached a maximum 21 days after flowering. This maximum was lower for heat stress variants and decreased more rapidly. Heat stress can vary from year to year under field conditions. Since heat stress changes the ratio between embryo and endosperm DNA in the direction of a higher portion of embryo DNA at maturity, this has an influence on the measured content of GM DNA from GM pollen transfer into conventional maize fields.

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References

  • Amler R (2008) Beitrag zum Qualitäts- und Ertragspotenzial stress- und trockenheitstoleranter Sorten für Silo- und Energiemais bei optimaler Reife. Gesunde Pflanzen 60:5–13

    Article  Google Scholar 

  • Artlip TS, Madison JT, Setter TL (1995) Water deficit in developing endosperm of maize: cell division and nuclear DNA endoreduplication. Plant Cell Environ 18:1034–1040

    Article  CAS  Google Scholar 

  • Banerjee D, Pal SK (2008) Dynamics in DNA recognition by DAP: exploration of the various binding modes. J Phys Chem B 112:1016–1021

    Article  PubMed  CAS  Google Scholar 

  • Bennett MD (1995) Nuclear and chromosomal DNA amounts in Zea mays spp. mays. http://www.maizegdb.org/ancillary/zmdnaamt.html#Bir1993. Accessed 10 March 2010

  • Bennett MD, Leitch IJ (1995) Nuclear DNA amounts in angiosperms. Ann Botany 76:113–176

    Article  CAS  Google Scholar 

  • Biradar DP, Rayburn AL (1993) Heterosis and nuclear DNA content in maize. Heredity 71:300–304

    Article  Google Scholar 

  • Biradar DP, Rayburn AL, Bullock DG (1993) Endopolyploidy in diploid and tetraploid maize (Zea Mays L.). Ann Botany 71:417–421

    Article  Google Scholar 

  • Blacklow WM (1972) Influence of temperature on germination and elongation of the radicle and shoot of corn (Zea mays L.). Crop Sci 12:647–650

    Article  Google Scholar 

  • Brown RC, Lemmon BE (2007) The developmental biology of cereal endosperm. In: Olsen OA (ed) Developmental and molecular biology plant cell monographs, vol 8. Springer, Heidelberg, pp 1–20

    Google Scholar 

  • Cavallini A, Natali L, Balconi C, Rizzi E, Motto M, Cionini G, D’Amato F (1995) Chromosome endoreduplication in endosperm cells of two maize genotypes and their progenies. Protoplasma 189:156–162

    Article  Google Scholar 

  • Coelho CM, Dante RA, Sabelli PA, Sun Y, Dilkes BP, Gordon-Kamm WJ, Larkins BA (2005) Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication. Plant Physiol 138:2323–2336

    Article  PubMed  CAS  Google Scholar 

  • Devos Y, Reheul D, Schrijver ADE (2005) The co-existence between transgenic and non-transgenic maize in the European Union: a focus on pollen flow and cross-fertilization. Environ Biosafety Res 4:71–87

    Article  PubMed  Google Scholar 

  • Dilkes BP, Dante RA, Coelho C, Larkins BA (2002) Genetic analyses of endoreduplication in Zea mays endosperm: evidence of sporophytic and zygotic maternal control. Genetics 160:1163–1177

    PubMed  Google Scholar 

  • Dolezel J, Greihuber J, Suda J (2007a) Flow cytometry with plant cells: an overview. In: Dolezel J, Greihuber J, Suda J (eds) Flow cytometry with plant cells analysis of genes chromosomes and genomes. Wiley, New York, pp 41–65

    Google Scholar 

  • Dolezel J, Kubalakova M, Paux E, Bartos J, Feuillet C (2007b) Chromosome-based genomics in the cereals. Chromosome Res 15:51–66

    Article  PubMed  CAS  Google Scholar 

  • Ellis RE, Yuan J, Horvitz HR (1991) Mechanism and functions of cell death. Ann Rev Cell Biol 7:663–698

    Article  PubMed  CAS  Google Scholar 

  • Engelen-Eigles G, Jones RJ, Philips RL (2000) DNA endoreduplication in maize endosperm cells: the effect of exposure to short-term high temperature. Plant Cell Environ 23:657–663

    Article  CAS  Google Scholar 

  • Engelen-Eigles G, Jones RJ, Phillips RL (2001) DNA endoreduplication in maize endosperm cells is reduced by high temperature during the mitotic phase. Crop Sci 41:1114–1121

    Article  Google Scholar 

  • Gallagher SR, Desjardins PR (2008) Quantitation of DNA and RNA with absorption and fluorescence spectroscopy. Curr Protocols Protein Sci 4K.1–4K.21

  • Gesch RW, Archer DW (2005) Influence of sowing date on emergence characteristics of maize seed coated with a temperature-activated polymer. Agron J 97:1543–1550

    Article  Google Scholar 

  • Held PG (2001) Nucleic acid purity assessment using A260/A280 ratios, biotek application notes. http://www.biotek.com. Accessed 10 March 2010

  • Johnston JS, Bennet MD, Rayburn AL, Galbraith DW, Price HJ (1999) Reference standards for determination of DNA content of plant nuclei. Am J Botany 86:609–613

    Article  CAS  Google Scholar 

  • Kapuscinski J (1995) DAPI: a DNA-specific fluorescent probe. Biotech Histochem 70:220–223

    Article  PubMed  CAS  Google Scholar 

  • Kowles RV, Phillips RL (1985) DNA amplification patterns in maize endosperm nuclei during kernel development. PNAS 82:7010–7014

    Article  PubMed  CAS  Google Scholar 

  • Kowles RV, Srienc F, Phillips RL (1990) Endoreduplication of nuclear DNA in the developing maize endosperm. Develop Genet 11:125–132

    Article  CAS  Google Scholar 

  • Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo YM, Liu Y (2001) Investigating the hows and whys of DNA endoreduplication. J Exp Botany 52(355):183–192

    Article  CAS  Google Scholar 

  • Laurie D, Bennett MD (1985) Nuclear DNA content in the genera Zea and Sorghum. intergeneric, interspecific and intraspecific variation. Heredity 55:307–313

    Article  Google Scholar 

  • Leblanc O, Pointe C, Hernandez M (2002) Cell cycle progression during endosperm development in Zea mays depends on parental dosage effects. Plant J 32:1057–1066

    Article  PubMed  CAS  Google Scholar 

  • Lur HS, Setter T (1993) Role of auxin in maize endosperm evelopment. Plant Physiol 103:273–280

    PubMed  CAS  Google Scholar 

  • Marek SM, Wu J, Glass NL, Gilchrist DG, Bostock DG (2003) Nuclear DNA degradation during heterokaryon incompatibility in Neurospora crassa. Fungal Genet Biol 40:126–137

    Article  PubMed  CAS  Google Scholar 

  • Monjardino P, Smith AG, Jones RJ (2006) Zein transcription and endoreduplication in maize endosperm are differentially affected by heat stress. Crop Sci 46:2581–2589

    Article  CAS  Google Scholar 

  • Nguyen HN, Sabelli PA, Larkins RA (2007) Endoreduplicaion and programmed cell death in the cereal endosperm. In: Olsen OA (ed) Developmental and molecular biology plant cell monographs, vol 8. Springer, Heidelberg, pp 21–43

    Google Scholar 

  • Nicoletti I, Mannucci R, Migliorati G, Riccardi C, and Grignani F (1997) Common methods for measuring apoptotic cell death by flow cytometry. In: Cossarizza A (ed) Purdue Cytometry CD-ROM, vol 3. Purdue University, West Lafayette. http://www.cyto.purdue.edu/cdroms/flow/vol3/16/data/page3.htm

  • Ochatt SJ (2008) Flow cytometry in plant breeding. Cytometry A 73A:581–598

    Article  CAS  Google Scholar 

  • Pietramellara G, Ascher J, Ceccherini MT, Nannipieri P, Wenderoth D (2007) Adsorption of pure and dirty bacterial DNA on clay minerals and their transformation frequency. Biol Fertil Soils 43:731–739

    Article  CAS  Google Scholar 

  • Poggio L, Rosato M, Chiavarino AM, Naranjo CA (1998) Genome size and environmental correlations in maize (Zea mays ssp. mays, Poaceae). Ann Botany 82:107–115; (Supplement A)

  • Radchuk V, Borisjuk L, Radchuk R, Steinbiss HH, Rolletschek H, Broeders S, Wobus U (2006) Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell 18:1652–1666

    Article  PubMed  CAS  Google Scholar 

  • Rymen B, Fiorani F, Kartal F, Vandepoele K, Inze D, Beemster GTS (2007) Cold night impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol 143:1429–1438

    Article  PubMed  CAS  Google Scholar 

  • Schmid FX (2001) Biological macromolecules: UV–visible spectrophotometry. Encyclopedia Life Sci, introductory articles, 1–4. doi:10.1038/npg.els.0003142

  • Setter TL, Flannigan BA (2001) Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. J Exper Botany 52:1401–1408

    Article  CAS  Google Scholar 

  • Sun Y, Flanningan BA, Setter TL (1999) Regulation of endoreduplication in maize (Zea mays L.) endosperm: isolation of a novel B1-type cyclin and its quantitative analysis. Plant Mol Biol 41:245–258

    Article  PubMed  CAS  Google Scholar 

  • Tarnowski BI, Spinale FG, Nicholson JH (1991) DAPI as a useful stain for nuclear quantification. Biotech Histochem 66:297–302

    Article  PubMed  CAS  Google Scholar 

  • Trifa Y, Zhang D (2004) DNA content in embryo and endosperm of maize kernel (Zea mays L.): impact on GMO quantification. J Agric Food Chem 52:1044–1048

    Article  PubMed  CAS  Google Scholar 

  • Weber WE (2008) Can GM and organic agriculture coexist? CAB reviews: Persp Agric Veter Sci Nutr Natur Res. 3/72:1–8. doi:10.1079/PAVSNNR20083072

  • Weber WE, Bringezu T, Broer I, Eder J, Holz F (2007) Coexistence between GM and non-GM maize crops tested in 2004 at the field scale level (Erprobungsanbau 2004). J Agron Crop Sci 193:79–92

    Article  CAS  Google Scholar 

  • Wilhelm EP, Mullen RE, Keeling PL, Singletary GW (1999) Heat stress during grain filling in maize: effects on kernel growth and metabolism. Crop Sci 39:1733–1741

    Article  CAS  Google Scholar 

  • Yanpaisan W, King NJC, Doran PM (1999) Flow cytometry of plant cells with applications in large-scale bioprocessing. Biotechn Adv 17:3–27

    Article  CAS  Google Scholar 

  • Young TE, Gallie D (2000) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301

    Article  PubMed  CAS  Google Scholar 

  • Young TE, Callie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115:737–751

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grant of the Deutsche Forschungsgemeinschaft (DFG), project number WE 647/15-1.

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Authors and Affiliations

  1. Plant Breeding, Institute of Agricultural and Nutritional Sciences, Martin-Luther-University Halle-Wittenberg, Betty-Heimann-Str. 5, 06120, Halle/Saale, Germany

    T. G. G. Bringezu & W. E. Weber

  2. Apomixis Research Group, Department of Cytogenetics and Genome Analysis, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), 06466, Gatersleben, Germany

    T. F. Sharbel

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  1. T. G. G. Bringezu
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  2. T. F. Sharbel
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  3. W. E. Weber
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Correspondence to W. E. Weber.

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Bringezu, T.G.G., Sharbel, T.F. & Weber, W.E. Grain development and endoreduplication in maize and the impact of heat stress. Euphytica 182, 363–376 (2011). https://doi.org/10.1007/s10681-011-0506-y

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