Abstract
It has been demonstrated that insertion of foreign DNA into mammalian genome can profoundly alter the patterns of DNA methylation and transcription of the host genome. Introgression of alien DNA into plant genomes through sexual crossing and genetic engineering are commonly used in breeding, but it is not known if plant genomes have similar responses to alien DNA introgression as those of animals. Two stable rice lines with introgression from wild rice, Zizania latifolia, were analyzed for patterns of cytosine DNA methylation and transcription of a set of selected sequences, including cellular genes and transposable element (TE)-related DNA segments. In 21 of the 30 studied sequences, marked changes in DNA methylation and/or transcription were observed compared with those of the rice parent. In all analyzed sequences, the absence of Zizania homologues in the introgression lines was confirmed. No change in DNA methylation and expression patterns was detected in randomly selected individuals of the rice parent nor in two sibling lines without introgressed Zizania DNA. The changed methylation patterns in both introgression lines were stably maintained in all five randomly sampled individuals of a given line, as well as in selfed progenies of the lines. Changed patterns in methylation and expression were also found in an independently produced asymmetric somatic nuclear hybrid (SH6) of rice and Z. latifolia that involves a different rice genotype but also contains a small amount of Z. latifolia DNA integrated into the rice genome. Thus, we have demonstrated that alien DNA introgression into a plant genome can induce extensive alterations in DNA methylation and transcription of both cellular genes and TE-related DNA segments in a genotype-independent manner.
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Adams, K.L., Cronn, R., Percifield, R. and Wendel, J.F. 2003. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl. Acad. Sci. USA 100: 4649–4654.
Arnold, M.L. 1997. Natural Hybridizatio and Evolution. Oxford University Press, New York.
Cox, A.V., Bennett, S.T., Parokonny, A.S., Kenton, A., Callimassia, M.A. and Bennett, M.D. 1993. Comparision of plant telomeres using PCR-generated synthetic probes. Ann. Bot. 72: 239–247.
Cronn, R. and Wendel, J.F. 2003. Cryptic trysts, genomic mergers, and plant speciation. New Phytol. 161: 133–142.
Finnegan, E.J., Peacock, W.J. and Dennis, E.S. 2000. DNA methylation, a key regulator of plant development and other processes. Curr. Opin. Genet. Dev. 10: 217–223.
Grandibastien, M.A. 1998. Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3: 181–187.
Hashida, S.N., Kitamura, K., Mikami, T. and Kishima, Y. 2003. Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 in Antirrhinum majus. Plant Physiol. 132: 1207–1216.
Heller, H., Kammer, C., Wilgenbus, P. and Doerfler, W. 1995. The chromosomal insertion of foreign (adenovirus type 12, plasmid of bacteriaphage) DNA is associated with enhanced methylation of cellular DNA segments. Proc. Natl. Acad. Sci. USA 92: 5515–5519.
Hirochika, H., Fukuchi, A. and Kikuchi, F. 1992. Retrotransposon families in rice. Mol. Gen. Genet. 233: 209–216.
Ivashuta, S., Naumkina, M., Gau, M., Uchiyama, K., Isobe, S., Mizukami, Y. and Shimamoto, Y. 2002. Genotype-dependent transcriptional activation of novel repetitive elements during cold acclimation of alfalfa (Medicago sativa). Plant J. 31: 615–627.
Jeddeloh, J.A., Stokes, T.L. and Richards, E.J. 1999. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat. Genet. 22: 94–97.
Lindroth, A.M., Cao, X., Jackson, J.P., Zilberman, D., McCallum, C.M., Heniko, S. and Jacobsen, S.E. 2001. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077–2080.
Kaeppler, S.M. and Phillips, R.L. 1993. Tissue culture-induced DNA methylation variations in maize. Proc. Natl. Acad. Sci. USA 90: 8773–8776.
Liu, B., Piao, H.M., Zhao. F.S., Zhao, J.H. and Zhao, R. 1999a. Production and molecular characterization of rice lines with introgressed traits from a wild species of Zizania latifolia Griseb. J. Genet. Breed. 53: 279–284.
Liu, B., Liu, Z.L. and Li X.W. 1999b. Production of a highly asymmetric somatic hybrid between rice and Zizania latifolia: evidence for inter-genomic exchange. Theor. Appl. Genet. 98: 1099–1103.
Luff, B., Pawlowski, L. and Bender, J. 1999. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3: 505–511.
Matzke, M.A., Aufsatz, W., Kanno, T., Mette, M. F. and Matzke, A.J. 2002. Homology-dependent gene silencing and host defense in plants. Adv. Genet. 46: 235–275.
Melquist, S., Luff, B. and Bender, J. 1999. Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genetics 153: 401–413.
Muller, K., Heller, H. and Doerfler, W. 2001. Foreign DNA integration. Genome-wide perturbations of methylation and transcription in the recipient genomes. J. Biol. Chem. 276: 14271–14278.
Remus, R., Kammer, C., Heller, H., Schemitz, B., Schell, G. and Doerfler, W. 1999. Insertion of foreign DNA into an established mammalian genome can alter the methylation of cellular DNA sequences. J. Virol. 73: 1010–1022.
Rieseberg, L.H. 1995. The role of hybridization in evolution: old wine in new skins. Am. J. Bot. 82: 944–953.
Rieseberg, L.H., Baird, S.J.E. and Gardner, K. 2000. Hybridization, introgression, and linkage evolution. Plant Mol. Biol. 42: 205–224.
Rieseberg, L.H., Widmer, A., Arntz, A.M. and Burke, J. M. 2003. The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358: 1141–1147.
Steward, N., Ito, M., Yamaguchi, Y., Koizumi, N. and Sano, H. 2002. Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J. Biol. Chem. 277: 37741–37746.
Van Driel, R., Fransz, P. F. and Verschure, P.J. 2003. The eukaryotic genome: a system regulated at different hierarchical levels. J. Cell Sci. 116: 4067–4075.
Wendel, J.F. 2000. Genome evolution in polyploids. Plant Mol. Biol. 42: 225–249.
Wessler, S.R. 1996. Plant retrotransposons: turned on by stress. Cur. Biol. 6: 959–961.
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Liu, Z., Wang, Y., Shen, Y. et al. Extensive Alterations in DNA Methylation and Transcription in Rice Caused by Introgression from Zizania Latifolia . Plant Mol Biol 54, 571–582 (2004). https://doi.org/10.1023/B:PLAN.0000038270.48326.7a
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DOI: https://doi.org/10.1023/B:PLAN.0000038270.48326.7a