Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1999 Jun;11(6):1047–1060. doi: 10.1105/tpc.11.6.1047

Transgenic tobacco plants expressing the Drosophila Polycomb (Pc) chromodomain show developmental alterations: possible role of Pc chromodomain proteins in chromatin-mediated gene regulation in plants.

R Ingram 1, B Charrier 1, C Scollan 1, P Meyer 1
PMCID: PMC144239  PMID: 10368176

Abstract

The chromodomain of the Drosophila Polycomb (Pc) protein has been introduced into tobacco nuclei to determine its location in the nucleus and its effect on plant development. Pc is a repressor of homeotic Drosophila genes that shares a well-conserved, although not identical, chromodomain with a structural heterochromatin component, Heterochromatin Protein 1. The chromodomains might therefore play a common role in chromatin repression. An analysis of transgenic plants expressing the Pc chromodomain, which was linked to the green fluorescent protein, suggested that the Pc chromodomain has distinct target regions in the plant genome. Transgenic plants expressing the Pc chromodomain had phenotypic abnormalities in their leaves and flowers, indicating a disruption in development. In axillary shoot buds of plants displaying altered leaf phenotypes, enhanced expression of a homeodomain gene, which is downregulated in wild-type leaves, was found. In Drosophila, Pc has been shown to possess distinct chromosome binding activity and to be involved in the regulation of development-specific genes. Our results support the assumptions that the heterologous chromodomain affects related functions in Drosophila and in plants, and that chromatin modification mechanisms are involved in the regulation of certain plant genes, in a manner similar to chromatin-mediated gene regulation in Drosophila.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Chalfie M., Tu Y., Euskirchen G., Ward W. W., Prasher D. C. Green fluorescent protein as a marker for gene expression. Science. 1994 Feb 11;263(5148):802–805. doi: 10.1126/science.8303295. [DOI] [PubMed] [Google Scholar]
  2. DeCamillis M., Cheng N. S., Pierre D., Brock H. W. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb. Genes Dev. 1992 Feb;6(2):223–232. doi: 10.1101/gad.6.2.223. [DOI] [PubMed] [Google Scholar]
  3. Dorer D. R., Henikoff S. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell. 1994 Jul 1;77(7):993–1002. doi: 10.1016/0092-8674(94)90439-1. [DOI] [PubMed] [Google Scholar]
  4. Dreesen T. D., Henikoff S., Loughney K. A pairing-sensitive element that mediates trans-inactivation is associated with the Drosophila brown gene. Genes Dev. 1991 Mar;5(3):331–340. doi: 10.1101/gad.5.3.331. [DOI] [PubMed] [Google Scholar]
  5. Franke A., DeCamillis M., Zink D., Cheng N., Brock H. W., Paro R. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 1992 Aug;11(8):2941–2950. doi: 10.1002/j.1460-2075.1992.tb05364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Freeling M. A conceptual framework for maize leaf development. Dev Biol. 1992 Sep;153(1):44–58. doi: 10.1016/0012-1606(92)90090-4. [DOI] [PubMed] [Google Scholar]
  7. Goodrich J., Puangsomlee P., Martin M., Long D., Meyerowitz E. M., Coupland G. A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature. 1997 Mar 6;386(6620):44–51. doi: 10.1038/386044a0. [DOI] [PubMed] [Google Scholar]
  8. Hake S. Unraveling the knots in plant development. Trends Genet. 1992 Mar;8(3):109–114. doi: 10.1016/0168-9525(92)90199-e. [DOI] [PubMed] [Google Scholar]
  9. Henikoff S., Comai L. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics. 1998 May;149(1):307–318. doi: 10.1093/genetics/149.1.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. James T. C., Elgin S. C. Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol. 1986 Nov;6(11):3862–3872. doi: 10.1128/mcb.6.11.3862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kaelin W. G., Jr, Krek W., Sellers W. R., DeCaprio J. A., Ajchenbaum F., Fuchs C. S., Chittenden T., Li Y., Farnham P. J., Blanar M. A. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell. 1992 Jul 24;70(2):351–364. doi: 10.1016/0092-8674(92)90108-o. [DOI] [PubMed] [Google Scholar]
  12. Kennison J. A. The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu Rev Genet. 1995;29:289–303. doi: 10.1146/annurev.ge.29.120195.001445. [DOI] [PubMed] [Google Scholar]
  13. Lincoln C., Long J., Yamaguchi J., Serikawa K., Hake S. A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell. 1994 Dec;6(12):1859–1876. doi: 10.1105/tpc.6.12.1859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mandel T., Lutziger I., Kuhlemeier C. A ubiquitously expressed MADS-box gene from Nicotiana tabacum. Plant Mol Biol. 1994 May;25(2):319–321. doi: 10.1007/BF00023247. [DOI] [PubMed] [Google Scholar]
  15. Matsuoka M., Ichikawa H., Saito A., Tada Y., Fujimura T., Kano-Murakami Y. Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell. 1993 Sep;5(9):1039–1048. doi: 10.1105/tpc.5.9.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Matzke M. A., Matzke AJM. How and Why Do Plants Inactivate Homologous (Trans)genes? Plant Physiol. 1995 Mar;107(3):679–685. doi: 10.1104/pp.107.3.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matzke M. A., Primig M., Trnovsky J., Matzke A. J. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J. 1989 Mar;8(3):643–649. doi: 10.1002/j.1460-2075.1989.tb03421.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Messmer S., Franke A., Paro R. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 1992 Jul;6(7):1241–1254. doi: 10.1101/gad.6.7.1241. [DOI] [PubMed] [Google Scholar]
  19. Meyer P., Heidmann I., Niedenhof I. Differences in DNA-methylation are associated with a paramutation phenomenon in transgenic petunia. Plant J. 1993 Jul;4(1):89–100. doi: 10.1046/j.1365-313x.1993.04010089.x. [DOI] [PubMed] [Google Scholar]
  20. Meyer P., Niedenhof I., ten Lohuis M. Evidence for cytosine methylation of non-symmetrical sequences in transgenic Petunia hybrida. EMBO J. 1994 May 1;13(9):2084–2088. doi: 10.1002/j.1460-2075.1994.tb06483.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Meyer P., Saedler H. HOMOLOGY-DEPENDENT GENE SILENCING IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):23–48. doi: 10.1146/annurev.arplant.47.1.23. [DOI] [PubMed] [Google Scholar]
  22. Müller J. Transcriptional silencing by the Polycomb protein in Drosophila embryos. EMBO J. 1995 Mar 15;14(6):1209–1220. doi: 10.1002/j.1460-2075.1995.tb07104.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Paro R., Hogness D. S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):263–267. doi: 10.1073/pnas.88.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Paro R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 1990 Dec;6(12):416–421. doi: 10.1016/0168-9525(90)90303-n. [DOI] [PubMed] [Google Scholar]
  25. Pickett F. B., Champagne M. M., Meeks-Wagner D. R. Temperature-sensitive mutations that arrest Arabidopsis shoot development. Development. 1996 Dec;122(12):3799–3807. doi: 10.1242/dev.122.12.3799. [DOI] [PubMed] [Google Scholar]
  26. Pirrotta V., Rastelli L. White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila. Bioessays. 1994 Aug;16(8):549–556. doi: 10.1002/bies.950160808. [DOI] [PubMed] [Google Scholar]
  27. Schneeberger R. G., Becraft P. W., Hake S., Freeling M. Ectopic expression of the knox homeo box gene rough sheath1 alters cell fate in the maize leaf. Genes Dev. 1995 Sep 15;9(18):2292–2304. doi: 10.1101/gad.9.18.2292. [DOI] [PubMed] [Google Scholar]
  28. Simon J. Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr Opin Cell Biol. 1995 Jun;7(3):376–385. doi: 10.1016/0955-0674(95)80093-x. [DOI] [PubMed] [Google Scholar]
  29. ten Lohuis M., Müller A., Heidmann I., Niedenhof I., Meyer P. A repetitive DNA fragment carrying a hot spot for de novo DNA methylation enhances expression variegation in tobacco and petunia. Plant J. 1995 Dec;8(6):919–932. doi: 10.1046/j.1365-313x.1995.8060919.x. [DOI] [PubMed] [Google Scholar]
  30. van Blokland R., ten Lohuis M., Meyer P. Condensation of chromatin in transcriptional regions of an inactivated plant transgene: evidence for an active role of transcription in gene silencing. Mol Gen Genet. 1997 Dec;257(1):1–13. doi: 10.1007/s004380050617. [DOI] [PubMed] [Google Scholar]
  31. van der Krol A. R., Chua N. H. The basic domain of plant B-ZIP proteins facilitates import of a reporter protein into plant nuclei. Plant Cell. 1991 Jul;3(7):667–675. doi: 10.1105/tpc.3.7.667. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES