Abstract
Hexaploid wheat (Triticum aestivum) contains triplicated genomes derived from three distinct species. To better understand how different genomes are coordinated in the same nucleus of the hexaploid wheat, we globally compared gene expression of a synthetic hexaploid wheat with its diploid (Aegilops tauschii) and tetraploid (T. turgidum) parents by cDNA-AFLP display. The results suggested that the expression of a significant fraction of genes was altered in the synthetic hexaploid; most appeared to be diminished and some were activated. We characterized nine cDNA clones in details. Cytogenetic as well as genomic sequence analyses indicated that the gene silencing was not due to chromosome/DNA loss but was caused by gene regulation. Northern and RT-PCR divided these genes into three groups: (I) four genes were down-regulated nonspecifically, likely involving both parental orthologues; (II) four genes were down-regulated in an orthologue-dependent manner; (III) one gene was activated specifically in the synthetic hexaploid wheat. These genes were often altered non-randomly in different synthetic hexaploids as well as natural hexaploid wheat, suggesting that many of the gene expression changes were intrinsically associated with polyploidy.
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References
Averett, J.E. 1980. Polyploidy in plant taxa: summary. In: W.H. Lewis (Ed.) Polyploidy: Biological Relevance, Plenum Press, New York.
Bachem, C.W.B., van der Hoeven, R.S., de Bruijn, S.M., Vreugdenhil, D., Zabeau, M. and Visser, R.G.F. 1996. Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J. 9: 745–753.
Blanc, G., Barakat, A., Guyot, R., Cooke, R. and Delseny, D. 2000. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12: 1093–1101.
Comai, L., Tyagi, A.P., Winter, K., Holmes-Davis, R., Reynolds, S.H., Stevens, Y. and Byers, B. 2000. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12: 1551–1568.
Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. and Jones, J.D.G. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12: 963–977.
Dvorak, J. 1998. Genome analysis in the Triticum-Aegilops alliance. In: A.E. Slinkard (Ed.) Proceedings of the 9th International Wheat Genetics Symposium (Saskatoon, Saskatchewan, Canada) 1: 8–11. University Extension Press, University of Saskatchewan.
Feldman, M., Galili, G. and Levy, A.A. 1986. Genetic and evolutionary aspects of allopolyploidy in wheat. In: C. Barigozzi (Ed.) The Origin and Domestication of Cultivated Plants, Elsevier Science, New York, pp. 83–100.
Friebe, B. and Gill, B.S. 1994. C-band polymorphism and structural rearrangements detected in common wheat (Triticum aestivum). Euphytica 78: 1–5.
Friebe, B., Mukai, Y. and Gill, B.S. 1992. C-banding polymorphisms in several accessions of Triticum tauschii (Aegilops squarrosa). Genome 35: 192–199.
Galili, G. and Feldman, M. 1983. Diploidization of endosperm protein genes in polyploid wheats. In: Proceedings of the 6h International Wheat Genetics Symposium (Saskatoon, Saskatchewan, Canada), pp. 1119–1123. University Extension Press, University of Saskatchewan.
Galili, G. and Feldman, M. 1984. Intergenomic suppression of endosperm protein genes in common wheat. Can. J. Genet. Cytol. 26: 651–656.
Galitski, T., Saldanha, A.J., Styles, C.A., Lander, E.S. and Fink, G.R. 1999. Ploidy regulation of gene expression. Science 285: 251–254.
Gill, B.S. 1991. Nucleo-cytoplasmic interaction (NCI) hypothesis of genome evolution and speciation in polyploid plants. In: T. Sasakuma and T. Kinoshita (Eds.) Nuclear and Organellar Genomes of Wheat Species, Kihara Memorial Foundation, Yokohama, Japan, pp. 48–53.
Gill, B.S. and Friebe, B. 2002. Cytogenetics, phylogeny and evolution of cultivated wheats. In: B. Curtis (Ed.) Wheat Improvement, FAO, in press.
Guo, M., Davis, D. and Birchler, J.A. 1996. Dosage effects on gene expression in a maize ploidy series. Genetics 142: 1349–1355.
Hart, G.E. 1979. Evidence for a triplicate set of glucosephosphate isomerase structural genes in hexaploid wheat. Biochem. Genet. 17: 585–598.
Hart, G.E. 1996. Genome analysis in the Triticeae using isozymes. In: P.J. Jauhar (Ed.) Methods of Genome Analysis in Plants, CRC Press, Boca Raton, FL, pp. 195–209.
Huang, S., Sirikhachornkit, A., Su, X., Faris, J., Gill, B.S., Haselkorn, B. and Gornicki, P. 2002. Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of wheat. Proc. Natl. Acad. Sci. USA 99: 8133–8138.
Heun, M., Schafer-Pregl, R., Klawan, D., Castagna, R., Accerbi, M., Borghi, B. and Salamini, F. 1997. Site of einkorn wheat domestication identified by DNA fingerprinting. Science 278: 1312–1314.
Imaizumi, T. Kanegae, T. and Wada, M. 2000. Cryptochrome nucleocytoplasmic distribution and gene expression are regulated by light quality in the fern Adiantum capillus-veneris. Plant Cell 12: 81–95.
Kashkush, K., Feldman, M. and Levy, A.A. 2002. Gene loss, silencing and activation in newly synthesized wheat allotetraploid. Genetics 160: 1651–1659.
Ku, H.-M., Vision, T., Liu, J. and Tanksley, S.D. 2000. Comparing sequenced segments of the tomato and Arabidopsis genomes: large scale duplication followed by selective gene loss creates a network of synteny. Proc. Natl. Acad. Sci. USA 97: 9121–9126.
Lee, H.-S. and Chen, Z.J. 2001. Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc. Natl. Acad. Sci. USA 98: 6753–6758.
Liu, B. Brubaker, C.L., Mergeai, G., Cronn, R.C. and Wendel, J.F. 2001. Polyploid formation in cotton is not accompanied by rapid genomic changes. Genome 44: 321–330.
Liu, B., Vega, J.M., and Feldman, M. 1998. Rapid genome changes in newly synthesized amphiploids of Triticum and Aegilops. II. Changes in low-copy coding DNA sequences. Genome 41: 535–542.
MacFadden, E.S. and Sears, E.R. 1944. The artificial synthesis of Triticum spelta. Rec. Soc. Genet. Am. 13: 26–27.
MacFadden, E.S. and Sears, E.R. 1946. The Origin of Triticum spelta and its free-threshing hexaploid relatives. J. Hered. 37: 81–69, 107–116.
Madlung, A., Masuelli, R.W., Watson, B., Reynolds, S.H., Davison, J. and Comai, L. 2002. Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol. 129: 733–746.
McClintock, B. 1984. The significance of responses of the genome to challenge. Science 226: 792–801.
McIntosh, R.A., Hart, G.E., Devos, K.M., Gale, M.D. and Rogers, W.J. 1998. Catalogue of gene symbols for wheat. Proceedings of the 9th International Wheat Genetics Symposium (Saskatoon, Saskatchewan, Canada), 5. University Extension Press, University of Saskatchewan.
Mittelsten-Scheid, O., Jakovleva, L., Afsar, K., Maluszynska, J., Paszkowski, J. 1996. A change in ploidy can modify epigenetic silencing. Proc. Natl. Acad. Sci. USA 93: 7114–7119.
Mukai, Y., Endo, T.R. and Gill, B.S. 1991. Physical mapping of the 18S-26S rRNA multigene family in common wheat: identification of a new locus. Chromosoma 100: 71–78.
Nelson, J.C., Deynze A.E.V., Autrique, E., Sorrells, Lu, Y.H., Merlino, M., Atkinson, M. and Leroy, P. 1995. Molecular mapping of wheat homoeologous group 2. Genome 38: 516–524.
Ozkan, H., Levy, A.A. and Feldman, M. 2001. Allopolyploidyinduced rapid genome evolution in the wheat (Aegilops-Triticum) group. Plant Cell 13: 1735–1747.
Sakamoto, S. 1973. Patterns of phylogenetic differentiation in the tribe Triticeae. Seiken Ziho 24: 11–31.
Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Shaked, H., Kashkush, K., Ozkan, H., Feldman, M. and Levy, A.A. 2001. Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13: 1749–1759.
Song, K., Lu, P., Tang, K. and Osborn, T.C. 1995. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc. Natl. Acad. Sci. USA 92: 7719–7723.
Wendel, J.F. 2000. Genome evolution in polyploids. Plant Mol. Biol. 42: 225–249.
Wolfe, K.H. and Shields, D.C. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708–713.
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He, P., Friebe, B.R., Gill, B.S. et al. Allopolyploidy alters gene expression in the highly stable hexaploid wheat. Plant Mol Biol 52, 401–414 (2003). https://doi.org/10.1023/A:1023965400532
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DOI: https://doi.org/10.1023/A:1023965400532