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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Jun 29;358(1434):1105–1111. doi: 10.1098/rstb.2003.1292

Imprinting in the endosperm: a possible role in preventing wide hybridization.

Jose F Gutierrez-Marcos 1, Paul D Pennington 1, Liliana M Costa 1, Hugh G Dickinson 1
PMCID: PMC1693205  PMID: 12831476

Abstract

Reproductive isolation is considered to play a key part in evolution, and plants and animals have developed a range of strategies that minimize gene flow between species. In plants, these strategies involve either pre-zygotic barriers, such as differences in floral structure and pollen-stigma recognition, or post-zygotic barriers, which are less well understood and affect aspects of seed development ranging from fertilization to maturation. In most angiosperms, a double fertilization event gives rise to a zygote and the endosperm: a triploid tissue with an unequal parental genomic contribution, which, like the placenta of mammals, provides reserves to the developing embryo. Interestingly, many aspects of endosperm development, again like the placenta, are regulated by a range of epigenetic mechanisms that are globally termed imprinting. Imprinted genes are characterized by their uniparental expression, the other parental allele being silenced. Normal development of the endosperm thus requires a highly specific balance of gene expression, from either the maternal or paternal genomes. Any alteration of this balance resulting from changes in allelic copy number, sequence or epigenetic imprints can cause endosperm failure and eventual seed abortion. In its widest sense, the endosperm thus serves as an accurate 'sensor' of compatibility between parents. A first step in understanding this important, yet complex system must clearly be the isolation and characterization of as wide a range as possible of imprinted genes.

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Selected References

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  1. Baroux Célia, Spillane Charles, Grossniklaus Ueli. Genomic imprinting during seed development. Adv Genet. 2002;46:165–214. doi: 10.1016/s0065-2660(02)46007-5. [DOI] [PubMed] [Google Scholar]
  2. Berger Frédéric. Endosperm: the crossroad of seed development. Curr Opin Plant Biol. 2003 Feb;6(1):42–50. doi: 10.1016/s1369526602000043. [DOI] [PubMed] [Google Scholar]
  3. Bhattramakki Dinakar, Dolan Maureen, Hanafey Mike, Wineland Robin, Vaske Dave, Register James C., 3rd, Tingey Scott V., Rafalski Antoni. Insertion-deletion polymorphisms in 3' regions of maize genes occur frequently and can be used as highly informative genetic markers. Plant Mol Biol. 2002 Mar-Apr;48(5-6):539–547. doi: 10.1023/a:1014841612043. [DOI] [PubMed] [Google Scholar]
  4. Birchler J. A. Dosage analysis of maize endosperm development. Annu Rev Genet. 1993;27:181–204. doi: 10.1146/annurev.ge.27.120193.001145. [DOI] [PubMed] [Google Scholar]
  5. Birchler J. A., Hart J. R. Interaction of endosperm size factors in maize. Genetics. 1987 Oct;117(2):309–317. doi: 10.1093/genetics/117.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chaudhuri S., Messing J. Allele-specific parental imprinting of dzr1, a posttranscriptional regulator of zein accumulation. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4867–4871. doi: 10.1073/pnas.91.11.4867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Choi Yeonhee, Gehring Mary, Johnson Lianna, Hannon Mike, Harada John J., Goldberg Robert B., Jacobsen Steven E., Fischer Robert L. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell. 2002 Jul 12;110(1):33–42. doi: 10.1016/s0092-8674(02)00807-3. [DOI] [PubMed] [Google Scholar]
  8. Cooper D C, Brink R A. Seed Collapse following Matings between Diploid and Tetraploid Races of Lycopersicon Pimpinellifolium. Genetics. 1945 Jul;30(4):376–401. doi: 10.1093/genetics/30.4.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cooper D. C., Brink R. A. Somatoplastic Sterility as a Cause of Seed Failure after Interspecific Hybridization. Genetics. 1940 Nov;25(6):593–617. doi: 10.1093/genetics/25.6.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cooper D. C., Brink R. A. THE ENDOSPERM AS A BARRIER TO INTERSPECIFIC HYBRIDIZATION IN FLOWERING PLANTS. Science. 1942 Jan 16;95(2455):75–76. doi: 10.1126/science.95.2455.75. [DOI] [PubMed] [Google Scholar]
  11. Danilevskaya Olga N., Hermon Pedro, Hantke Sabine, Muszynski Michael G., Kollipara Krishna, Ananiev Evgueni V. Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell. 2003 Feb;15(2):425–438. doi: 10.1105/tpc.006759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Evans M. M., Kermicle J. L. Interaction between maternal effect and zygotic effect mutations during maize seed development. Genetics. 2001 Sep;159(1):303–315. doi: 10.1093/genetics/159.1.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gavazzi G., Dolfini S., Allegra D., Castiglioni P., Todesco G., Hoxha M. Dap (Defective aleurone pigmentation) mutations affect maize aleurone development. Mol Gen Genet. 1997 Oct;256(3):223–230. doi: 10.1007/s004380050564. [DOI] [PubMed] [Google Scholar]
  14. Grimanelli D., Leblanc O., Perotti E., Grossniklaus U. Developmental genetics of gametophytic apomixis. Trends Genet. 2001 Oct;17(10):597–604. doi: 10.1016/s0168-9525(01)02454-4. [DOI] [PubMed] [Google Scholar]
  15. Grossniklaus U., Vielle-Calzada J. P., Hoeppner M. A., Gagliano W. B. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science. 1998 Apr 17;280(5362):446–450. doi: 10.1126/science.280.5362.446. [DOI] [PubMed] [Google Scholar]
  16. Gómez Elisa, Royo Joaquín, Guo Yan, Thompson Richard, Hueros Gregorio. Establishment of cereal endosperm expression domains: identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell. 2002 Mar;14(3):599–610. doi: 10.1105/tpc.010365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hagiwara Y., Hirai M., Nishiyama K., Kanazawa I., Ueda T., Sakaki Y., Ito T. Screening for imprinted genes by allelic message display: identification of a paternally expressed gene impact on mouse chromosome 18. Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9249–9254. doi: 10.1073/pnas.94.17.9249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jürgens G. Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J. 2001 Jul 16;20(14):3609–3616. doi: 10.1093/emboj/20.14.3609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kermicle J. L. Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics. 1970 Sep;66(1):69–85. doi: 10.1093/genetics/66.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kinoshita T., Yadegari R., Harada J. J., Goldberg R. B., Fischer R. L. Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell. 1999 Oct;11(10):1945–1952. doi: 10.1105/tpc.11.10.1945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lin B. Y. Association of endosperm reduction with parental imprinting in maize. Genetics. 1982 Mar;100(3):475–486. doi: 10.1093/genetics/100.3.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lin B. Y. Ploidy barrier to endosperm development in maize. Genetics. 1984 May;107(1):103–115. doi: 10.1093/genetics/107.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lund G., Ciceri P., Viotti A. Maternal-specific demethylation and expression of specific alleles of zein genes in the endosperm of Zea mays L. Plant J. 1995 Oct;8(4):571–581. doi: 10.1046/j.1365-313x.1995.8040571.x. [DOI] [PubMed] [Google Scholar]
  24. Lund G., Messing J., Viotti A. Endosperm-specific demethylation and activation of specific alleles of alpha-tubulin genes of Zea mays L. Mol Gen Genet. 1995 Mar 20;246(6):716–722. doi: 10.1007/BF00290717. [DOI] [PubMed] [Google Scholar]
  25. Luo M., Bilodeau P., Koltunow A., Dennis E. S., Peacock W. J., Chaudhury A. M. Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):296–301. doi: 10.1073/pnas.96.1.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Olsen Odd-Arne. ENDOSPERM DEVELOPMENT: Cellularization and Cell Fate Specification. Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52(NaN):233–267. doi: 10.1146/annurev.arplant.52.1.233. [DOI] [PubMed] [Google Scholar]
  27. Randolph L. F. Some Effects of High Temperature on Polyploidy and Other Variations in Maize. Proc Natl Acad Sci U S A. 1932 Mar;18(3):222–229. doi: 10.1073/pnas.18.3.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rhoades M. M., Dempsey E. Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics. 1966 Aug;54(2):505–522. doi: 10.1093/genetics/54.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Scholten Stefan, Lörz Horst, Kranz Erhard. Paternal mRNA and protein synthesis coincides with male chromatin decondensation in maize zygotes. Plant J. 2002 Oct;32(2):221–231. doi: 10.1046/j.1365-313x.2002.01418.x. [DOI] [PubMed] [Google Scholar]
  30. Scott R. J., Spielman M., Bailey J., Dickinson H. G. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development. 1998 Sep;125(17):3329–3341. doi: 10.1242/dev.125.17.3329. [DOI] [PubMed] [Google Scholar]
  31. Spielman M., Vinkenoog R., Dickinson H. G., Scott R. J. The epigenetic basis of gender in flowering plants and mammals. Trends Genet. 2001 Dec;17(12):705–711. doi: 10.1016/s0168-9525(01)02519-7. [DOI] [PubMed] [Google Scholar]
  32. Spillane C., MacDougall C., Stock C., Köhler C., Vielle-Calzada J. P., Nunes S. M., Grossniklaus U., Goodrich J. Interaction of the Arabidopsis polycomb group proteins FIE and MEA mediates their common phenotypes. Curr Biol. 2000 Nov 30;10(23):1535–1538. doi: 10.1016/s0960-9822(00)00839-3. [DOI] [PubMed] [Google Scholar]
  33. Springer Nathan M., Danilevskaya Olga N., Hermon Pedro, Helentjaris Tim G., Phillips Ronald L., Kaeppler Heidi F., Kaeppler Shawn M. Sequence relationships, conserved domains, and expression patterns for maize homologs of the polycomb group genes E(z), esc, and E(Pc). Plant Physiol. 2002 Apr;128(4):1332–1345. doi: 10.1104/pp.010742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Surani M. A. Reprogramming of genome function through epigenetic inheritance. Nature. 2001 Nov 1;414(6859):122–128. doi: 10.1038/35102186. [DOI] [PubMed] [Google Scholar]
  35. Sørensen M. B., Chaudhury A. M., Robert H., Bancharel E., Berger F. Polycomb group genes control pattern formation in plant seed. Curr Biol. 2001 Feb 20;11(4):277–281. doi: 10.1016/s0960-9822(01)00072-0. [DOI] [PubMed] [Google Scholar]
  36. Vielle-Calzada J. P., Baskar R., Grossniklaus U. Delayed activation of the paternal genome during seed development. Nature. 2000 Mar 2;404(6773):91–94. doi: 10.1038/35003595. [DOI] [PubMed] [Google Scholar]
  37. Vielle-Calzada J. P., Thomas J., Spillane C., Coluccio A., Hoeppner M. A., Grossniklaus U. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 1999 Nov 15;13(22):2971–2982. doi: 10.1101/gad.13.22.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vinkenoog R., Spielman M., Adams S., Fischer R. L., Dickinson H. G., Scott R. J. Hypomethylation promotes autonomous endosperm development and rescues postfertilization lethality in fie mutants. Plant Cell. 2000 Nov;12(11):2271–2282. doi: 10.1105/tpc.12.11.2271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yadegari R., Kinoshita T., Lotan O., Cohen G., Katz A., Choi Y., Katz A., Nakashima K., Harada J. J., Goldberg R. B. 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. 2000 Dec;12(12):2367–2382. doi: 10.1105/tpc.12.12.2367. [DOI] [PMC free article] [PubMed] [Google Scholar]

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