Imprinting in Maize

  • Nathan M. Springer
  • Jose F. Gutierrez-Marcos

Genomic imprinting in the maize endosperm results in differential expression of maternal and paternal alleles depending on their parental origin. The availability of sequence polymorphisms between different maize inbred lines and the large persistent endosperm of maize collectively provide a unique platform for studying the occurrence and mechanisms of imprinting in plants. Several imprinted genes have been identified in maize by targeted analyses. Genomic screens of allele-specific expression patterns in endosperm tissue have identified additional candidates for imprinting. Imprinted expression in maize is often associated with allele-specific DNA methylation states and it is likely that chromatin modifications are also involved in the establishment and maintenance of imprints.


Imprint Gene Endosperm Development Parental Allele Paternal Allele Maternal Allele 
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  1. Adams, S., Vinkenoog, R., Spielman, M., Dickinson, H.G., and R.J. Scott (2000) Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation. Development 127: 2493–2502.PubMedGoogle Scholar
  2. Alleman, M., and J. Doctor (2000) Genomic imprinting in plants: observations and evolutionary implications. Plant Mol Biol 43: 147–161.PubMedCrossRefGoogle Scholar
  3. Baroux, C., Pecinka, A., Fuchs, J., Schubert, I., and U. Grossniklaus (2007) The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell 19: 1782–1794.PubMedCrossRefGoogle Scholar
  4. Bianchi, M.W., and A. Viotti (1988) DNA methylation and tissue-specific transcription of the storage protein gene of maize. Plant Mol. Biol. 11: 203–214.CrossRefGoogle Scholar
  5. Brink, R.A., Kermicle, J.L., and N.K. Ziebur (1970) Derepression in the Female Gametophyte in Relation to Paramutant R Expression in Maize Endosperms, Embryos, and Seedlings. Genetics 66: 87–96.PubMedGoogle Scholar
  6. Chaudhuri, S., and J. Messing (1994) Allele-specific parental imprinting of dzr1, a posttranscrip-tional regulator of zein accumulation. Proc Natl Acad Sci U S A 91: 4867–4871.PubMedCrossRefGoogle Scholar
  7. Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B., Jacobsen, S.E., and R.L. Fischer (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell 110: 33–42.PubMedCrossRefGoogle Scholar
  8. Danilevskaya, O.N., Hermon, P., Hantke, S., Muszynski, M.G., Kollipara, K., and E.V. Ananiev (2003) Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15: 425–438.PubMedCrossRefGoogle Scholar
  9. Di Fonzo, N., Fornasari, E., Salamini, F., Reggiani, R., and C. Soave (1980) Interaction of maize mutants floury-2 and opaque-7 with opaque-2 in the synthesis of endosperm proteins. J. Hered. 71: 397–402.Google Scholar
  10. Dilkes, B.P., and L. Comai (2004) A differential dosage hypothesis for parental effects in seed development. Plant Cell 16: 3174–3180.PubMedCrossRefGoogle Scholar
  11. Gavazzi, G., Dolfini, S., Allegra, D., Castiglioni, P., Todesco, G., and M. Hoxha (1997) Dap (Defective aleurone pigmentation) mutations affect maize aleurone development. Mol Gen Genet 256: 223–230.PubMedCrossRefGoogle Scholar
  12. Gehring, M., Choi, Y., and R.L. Fischer (2004) Imprinting and seed development. Plant Cell 16Suppl: S203–213.PubMedCrossRefGoogle Scholar
  13. Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B., and R.L.Fischer (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124: 495–506.PubMedCrossRefGoogle Scholar
  14. Grimanelli, D., Perotti, E., Ramirez, J., and O. Leblanc (2005) Timing of the maternal-to-zygotic transition during early seed development in maize. Plant Cell 17: 1061–1072.PubMedCrossRefGoogle Scholar
  15. Guitton, A.E., and F. Berger (2005) Control of reproduction by Polycomb Group complexes in animals and plants. Int J Dev Biol 49: 707–716.PubMedCrossRefGoogle Scholar
  16. Guo, M., Rupe, M.A., Danilevskaya, O.N., Yang, X., and Z. Hu (2003) Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J 36: 30–44.PubMedCrossRefGoogle Scholar
  17. Gutierrez-Marcos, J.F., Pennington, P.D., Costa, L.M., and H.G. Dickinson (2003) Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos Trans R Soc Lond B Biol Sci 358: 1105–1111.PubMedCrossRefGoogle Scholar
  18. Gutierrez-Marcos, J.F., Costa, L.M., Dal Pra, M., Scholten, S., Kranz, E., Perez, P., and H.G. Dickinson (2006) Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet 38: 876–878.PubMedCrossRefGoogle Scholar
  19. Gutierrez-Marcos, J.F., Costa, L.M., Biderre-Petit, C., Khbaya, B., O'Sullivan, D.M., Wormald,M., Perez, P., and H.G. Dickinson (2004) maternally expressed gene1 Is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16: 1288–1301.PubMedCrossRefGoogle Scholar
  20. Haig, D., and M. Westoby (1989) Parent specific gene expression and the triploid endosperm. Am.Nat. 134: 147–155.CrossRefGoogle Scholar
  21. Haun, W.J., Laoueille-Duprat, S., O'Connell M, J., Spillane, C., Grossniklaus, U., Phillips, A.R.,Kaeppler, S.M., and N.M. Springer (2007) Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J 49: 325–337.PubMedCrossRefGoogle Scholar
  22. Hermon, P., Srilunchang, K.O., Zou, J., Dresselhaus, T., and O.N. Danilevskaya (2007) Activation of the imprinted Polycomb Group Fie1 gene in maize endosperm requires demethylation of the maternal allele. Plant Mol Biol 64: 387–395.PubMedCrossRefGoogle Scholar
  23. Howell, C.Y., Bestor, T.H., Ding, F., Latham, K.E., Mertineit, C., Trasler, J.M., and J.R. Chaillet (2001) Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104: 829–838.PubMedCrossRefGoogle Scholar
  24. Jeddeloh, J.A., Stokes, T.L., and E.J. Richards (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22: 94–97.PubMedCrossRefGoogle Scholar
  25. Jullien, P.E., Katz, A., Oliva, M., Ohad, N., and F. Berger (2006) Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol 16: 486–492.PubMedCrossRefGoogle Scholar
  26. Kermicle, J.L. (1970) Dependence of the R-Mottled Aleurone Phenotype in Maize on Mode of Sexual Transmission. Genetics 66: 69–85.PubMedGoogle Scholar
  27. Kermicle, J.L. (1978) Imprinting of gene action in maize endosperm. In: Maize breeding and Genetics (D.B. Walden, ed.) Wiley, New York, pp. 357–371.Google Scholar
  28. Kermicle, J.L., and M. Alleman (1990) Gametic imprinting in maize in relation to the angiosperm life cycle. Dev Suppl, 9–14.Google Scholar
  29. Kinoshita, T., Miura, A., Choi, Y., Kinoshita, Y., Cao, X., Jacobsen, S.E., Fischer, R.L., and T.Kakutani (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303: 521–523.PubMedCrossRefGoogle Scholar
  30. Kohler, C., and G. Makarevich (2006) Epigenetic mechanisms governing seed development in plants. EMBO Rep 7: 1223–1227.PubMedCrossRefGoogle Scholar
  31. Kohler, C., Page, D.R., Gagliardini, V., and U. Grossniklaus (2005) The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet 37: 28–30.PubMedGoogle Scholar
  32. Kohler, C., Hennig, L., Spillane, C., Pien, S., Gruissem, W., and U. Grossniklaus (2003) The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17: 1540–1553.PubMedCrossRefGoogle Scholar
  33. Lauria, M., Rupe, M., Guo, M., Kranz, E., Pirona, R., Viotti, A., and G. Lund (2004) Extensive maternal DNA hypomethylation in the endosperm of Zea mays. Plant Cell 16: 510–522.PubMedCrossRefGoogle Scholar
  34. Lund, G., Messing, J., and A. Viotti (1995a) Endosperm-specific demethylation and activation of specific alleles of alpha-tubulin genes of Zea mays L. Mol Gen Genet 246: 716–722.CrossRefGoogle Scholar
  35. Lund, G., Ciceri, P., and A. Viotti (1995b) Maternal-specific demethylation and expression of specific alleles of zein genes in the endosperm of Zea mays L. Plant J 8: 571–581.CrossRefGoogle Scholar
  36. McGinnis, K., Murphy, N., Carlson, A.R., Akula, A., Akula, C., Basinger, H., Carlson, M.,Hermanson, P., Kovacevic, N., McGill, M.A., Seshadri, V., Yoyokie, J., Cone, K., Kaeppler,H.F., Kaeppler, S.M., and N.M. Springer (2007) Assessing the efficiency of RNA interference for maize functional genomics. Plant Physiol 143: 1441–1451.PubMedCrossRefGoogle Scholar
  37. Messing, J., and H.K. Dooner (2006) Organization and variability of the maize genome. Curr Opin Plant Biol 9: 157–163.PubMedCrossRefGoogle Scholar
  38. Schwartz, D. (1965) Regulation of gene action in maize. In: Genetics Today (S.V. Geerst, ed.)Oxford, Pergamon, pp. 131–135.Google Scholar
  39. Selinger, D.A., and V.L. Chandler (2001) B-Bolivia, an allele of the maize b1 gene with variable expression, contains a high copy retrotransposon-related sequence immediately upstream. Plant Physiol 125M: 1363–1379.CrossRefGoogle Scholar
  40. Song, R., and J. Messing (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci U S A 100: 9055–9060.PubMedCrossRefGoogle Scholar
  41. Spillane, C., Schmid, K.J., Laoueille-Duprat, S., Pien, S., Escobar-Restrepo, J.M., Baroux, C.,Gagliardini, V., Page, D.R., Wolfe, K.H., and U. Grossniklaus (2007) Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448: 349–352.PubMedCrossRefGoogle Scholar
  42. Springer, N.M., Danilevskaya, O.N., Hermon, P., Helentjaris, T.G., Phillips, R.L., Kaeppler, H.F., and S.M. Kaeppler (2002) Sequence relationships, conserved domains, and expression patterns for maize homologs of the polycomb group genes E(z), esc, and E(Pc). Plant Physiol 128: 1332–1345.PubMedCrossRefGoogle Scholar
  43. Stupar, R.M., Hermanson, P.J., and N.M. Springer (2007) Non-additive Expression and Parent-of-origin Effects Identified by Microarray and Allele-specific Expression Profiling of Maize Endosperm. Plant Physiol. PMID: 17766400Google Scholar
  44. Vielle-Calzada, J.P., Thomas, J., Spillane, C., Coluccio, A., Hoeppner, M.A., and U. Grossniklaus (1999) Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev 13: 2971–2982.PubMedCrossRefGoogle Scholar
  45. Walter, J., and M. Paulsen (2003) The potential role of gene duplications in the evolution of imprinting mechanisms. Hum Mol Genet 12: R215–220.PubMedCrossRefGoogle Scholar
  46. Xiao, W., Brown, R.C., Lemmon, B.E., Harada, J.J., Goldberg, R.B., and R.L. Fischer (2006) Regulation of seed size by hypomethylation of maternal and paternal genomes. Plant Physiol 142: 1160–1168.PubMedCrossRefGoogle Scholar
  47. Xiao, W., Gehring, M., Choi, Y., Margossian, L., Pu, H., Harada, J.J., Goldberg, R.B., Pennell,R.I., and R.L. Fischer (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5: 891–901.PubMedCrossRefGoogle Scholar
  48. Yadegari, R., Kinoshita, T., Lotan, O., Cohen, G., Katz, A., Choi, Y., Nakashima, K., Harada, J.J.,Goldberg, R.B., Fischer, R.L., and N. Ohad (2000) Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms. Plant Cell 12: 2367–2382.PubMedCrossRefGoogle Scholar
  49. Zhao, J., and G. Grafi (2000) The high mobility group I/Y protein is hypophosphorylated in endoreduplicating maize endosperm cells and is involved in alleviating histone H1-mediated transcriptional repression. J Biol Chem 275: 27494–27499.PubMedGoogle Scholar

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© Springer Science + Business Media, LLC 2009

Authors and Affiliations

  1. 1.University of WarwickWarwick HRI

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