Imprinting of the Polycomb Group Gene MEDEA Serves As a Ploidy Sensor in Arabidopsis

Overview

Journal PLoS Genet

Specialty Genetics

Date 2009 Sep 26

PMID 19779546

Citations 64

Authors

Aleksandra Erilova

Lynette Brownfield

Vivien Exner

Marisa Rosa

David Twell

Ortrun Mittelsten Scheid

Lars Hennig

Claudia Kohler

Affiliations

Soon will be listed here.

Abstract

Balanced maternal and paternal genome contributions are a requirement for successful seed development. Unbalanced contributions often cause seed abortion, a phenomenon that has been termed "triploid block." Misregulation of imprinted regulatory genes has been proposed to be the underlying cause for abnormalities in growth and structure of the endosperm in seeds with deviating parental contributions. We identified a mutant forming unreduced pollen that enabled us to investigate direct effects of unbalanced parental genome contributions on seed development and to reveal the underlying molecular mechanism of dosage sensitivity. We provide evidence that parent-of-origin-specific expression of the Polycomb group (PcG) gene MEDEA is causally responsible for seed developmental aberrations in Arabidopsis seeds with increased paternal genome contributions. We propose that imprinted expression of PcG genes is an evolutionary conserved mechanism to balance parental genome contributions in embryo nourishing tissues.

Citing Articles

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References

Weijers D, Geldner N, Offringa R, Jurgens G . Seed development: Early paternal gene activity in Arabidopsis. Nature. 2001; 414(6865):709-10. DOI: 10.1038/414709a. View

Park S, Howden R, Twell D . The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development. 1998; 125(19):3789-99. DOI: 10.1242/dev.125.19.3789. View

Johnston S, den Nijs T, Peloquin S, Hanneman Jr R . The significance of genic balance to endosperm development in interspecific crosses. Theor Appl Genet. 2013; 57(1):5-9. DOI: 10.1007/BF00276002. View

Kinoshita T, Yadegari R, Harada J, Goldberg R, Fischer R . Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell. 1999; 11(10):1945-52. PMC: 144115. DOI: 10.1105/tpc.11.10.1945. View

Kohler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W . Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J. 2003; 22(18):4804-14. PMC: 212713. DOI: 10.1093/emboj/cdg444. View

Simon P . Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics. 2003; 19(11):1439-40. DOI: 10.1093/bioinformatics/btg157. View

Zhang X, Clarenz O, Cokus S, Bernatavichute Y, Pellegrini M, Goodrich J . Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 2007; 5(5):e129. PMC: 1852588. DOI: 10.1371/journal.pbio.0050129. View

Kohler C, Page D, Gagliardini V, Grossniklaus U . The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet. 2004; 37(1):28-30. DOI: 10.1038/ng1495. View

Leroy O, Hennig L, Breuninger H, Laux T, Kohler C . Polycomb group proteins function in the female gametophyte to determine seed development in plants. Development. 2007; 134(20):3639-48. DOI: 10.1242/dev.009027. View

10.

Kuzmin A, Han Z, Golding M, Mann M, Latham K, Varmuza S . The PcG gene Sfmbt2 is paternally expressed in extraembryonic tissues. Gene Expr Patterns. 2007; 8(2):107-16. PMC: 2220043. DOI: 10.1016/j.modgep.2007.09.005. View

11.

Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L . Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Curr Biol. 2009; 19(13):1128-32. PMC: 6754343. DOI: 10.1016/j.cub.2009.05.068. View

12.

Cooper D, Brink R . THE ENDOSPERM AS A BARRIER TO INTERSPECIFIC HYBRIDIZATION IN FLOWERING PLANTS. Science. 1942; 95(2455):75-6. DOI: 10.1126/science.95.2455.75. View

13.

Josefsson C, Dilkes B, Comai L . Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol. 2006; 16(13):1322-8. DOI: 10.1016/j.cub.2006.05.045. View

14.

Chaudhury A, Koltunow A, Payne T, Luo M, Tucker M, Dennis E . Control of early seed development. Annu Rev Cell Dev Biol. 2001; 17:677-99. DOI: 10.1146/annurev.cellbio.17.1.677. View

15.

Jullien P, Katz A, Oliva M, Ohad N, Berger F . Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol. 2006; 16(5):486-92. DOI: 10.1016/j.cub.2006.01.020. View

16.

Surani M, Barton S, Norris M . Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature. 1984; 308(5959):548-50. DOI: 10.1038/308548a0. View

17.

Costa L, Gutierrez-Marcos J, Dickinson H . More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci. 2004; 9(10):507-14. DOI: 10.1016/j.tplants.2004.08.007. View

18.

Jullien P, Mosquna A, Ingouff M, Sakata T, Ohad N, Berger F . Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol. 2008; 6(8):e194. PMC: 2504488. DOI: 10.1371/journal.pbio.0060194. View

19.

Haun W, Laoueille-Duprat S, OConnell M, Spillane C, Grossniklaus U, Phillips A . Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J. 2006; 49(2):325-37. DOI: 10.1111/j.1365-313X.2006.02965.x. View

20.

Marks G . THE ORIGIN AND SIGNIFICANCE OF INTRASPECIFIC POLYPLOIDY: EXPERIMENTAL EVIDENCE FROM SOLANUM CHACOENSE. Evolution. 2017; 20(4):552-557. DOI: 10.1111/j.1558-5646.1966.tb03385.x. View