Epigenetic aspects of sexual and asexual seed development

• Autorzy: Rodrigues J C M , Koltunow A.M.G.
• Języki publikacji: EN

Abstrakty

EN

In angiosperms, seed development initiates after a double fertilization event in the female gametophyte, in which one male sperm cell fuses to the central cell to form the endosperm and the other to the egg cell to form the embryo. Sexually-derived seed is thus characterized by maternal and paternal contributions to the progeny. Some plant species have the capacity to form seeds asexually, a process known as apomixis. This mode of reproduction is characterized by a bypass of meiotic reduction and the absence of paternal contribution to the embryo, resulting in a seed with an embryo genetically identical to the mother. Little is known about the molecular events that regulate apomictic development. Recent findings show that the apomictic and sexual developmental programs share molecular components, suggesting that apomixis is a deregulated sexual program. Furthermore, the identification of apomictic developmental features in fertilization-independent seed (fis) mutants in the sexual model plant Arabidopsis has also shed light on the molecular events that control sexual seed development, and has opened new questions as to the molecular nature of autonomous seed development. FIS-class genes are homologues of the Polycomb Group (PcG) chromatin remodelling factors conserved in Drosophila and humans, where they have been implicated in gene repression and control of cell fate throughout development. fis phenotypes are affected by DNA methylation, a DNA alteration associated with heterochromatin formation and gene silencing. Thus, the chromatin environment can be manipulated to make certain regions of the genome more or less susceptible to transcription; this form of control, in which gene expression patterns are altered without a change in the DNA sequence itself, is defined as epigenetic regulation. Different aspects of plant development have been shown to be controlled by epigenetic regulation. This review will highlight recent advances in understanding the epigenetic control of seed development. They are discussed in light of a model whereby altered epigenetic mechanisms might lead to complete maternal control of reproductive development as seen in apomixis.

Słowa kluczowe

EN

apomixia; asexual development; epigenetics; seed development; sexual development; plant

• Wydawca: -
• Czasopismo: Acta Biologica Cracoviensia. Series Botanica
• Rocznik: 2005
• Tom: 47
• Numer: 1
• Opis fizyczny: p.37-49,fig.,ref.

Twórcy

autor

Rodrigues J C M

• University of Adelaide, Glen Osmond, South Australia 5064, Australia

autor

Koltunow A.M.G.

Bibliografia

• Ach R, Taranto P, and Gruissem W. 1997. A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals. The Plant Cell 9: 1595-1606.
• Adams S, Vinkenoog R, Spielman M, Dickinson HG, and Scott RJ. 2000. Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation. Development 127: 2493-2502.
• Akiyama Y, Conner J, Goel S, Morishige D, Mullet J, Hanna W, and Ozias-Akins P. 2004. High-resolution physical mapping in Pennisetum squamulatum reveals extensive chromosomal heteromorphism of the genomic region associated with apomixis. Plant Physiology 134: 1733-1741.
• Asker SE, and Jerling L. 1992. Apomixis in plants. Boca Raton, CRC Press.
• Bao N, Lye K, and Barton M. 2004. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Developmental Cell 7: 653-662.
• Bastow R, Myine JS, Lister C, Lippman Z, Martienssen RA, and Dean C. 2004. Vernalization requires epigenetic silencing of FLC histone methylation. Nature 427:164-167.
• Baumbusch A, Thorstensen T, Kraus V, Fischer A, Naumann K, Assalkhou R, Schulz I, Reuter G, and Aalen RB. 2001. The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins tahta can be assigned to four evolutionarily conserved classes. Nucleic Acids Research 29: 4319-4333.
• Bestor T. 2000. The DNA methyltransferases of mammals. Human Molecular Genetics 9: 2395-2402.
• Bicknell R, and Kpltunow AM. 2004. Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16: S228-S245.
• Cao X, and Jacobsen SE. 2002. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. PNAS 99: 16491-16498.
• Cao X, and Jacobsen SE. 2002. Role of Arabdopsis DRM methyltransferases in De Novo DNA methylation and gene silencing. Current Biology 12: 1138-1144.
• Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, and Peacock WJ. 1997. Fertilization-independent seed development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the U.S.A. 94: 4223-4228.
• Choi YH, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, and Fischer RL. 2002. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110: 33-42.
• Ebel C, Mariconti L, and Gruissem W. 2004. Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429: 776-780.
• Ehrlich M. 2003. Expression of various genes is controlled by DNA methylation during mammalian development. Journal of Cellular Biochemistry 88: 899-910.
• Fergunson-Smith AC, and Surani M. 2001. Imprinting and the epigenetic asymmetry between parental genomes. Science 293: 1086-1089.
• Finnegan EJ, and Kovac KA. 2000. Plant DNA methyltransferases. Plant Molecular Biology 43: 189-201.
• Finnegan EJ, Peacock WJ, and Dennis ES. 1996. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proceedings of the National Academy of Sciences of the U.S.A. 93: 8449-8454.
• Francis NJ, and Kingston R. 2001. Mechanisms of transcriptional memory. Nature Reviews Molecular Cell Biology 2: 409-421.
• Gehring M, Choi Y, and Fischer RL. 2004. Imprinting and seed development. Plant Cell 16: S203-S213.
• Gendall AR, Levy YY, Wilson A, and Dean C. 2001. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107: 525-535.
• Genger RK, Kovac KA, Dennis ES, Peacock WJ, and Finnegan EJ. 1999. Multiple DNA methyltransferase genes in Arabidopsis thaliana. Plant Molecular Biology 41: 269-278.
• Genger RK, Peacock WJ, Dennis ES, and Finnegan EJ. 2003. Opposing effects of reduced DNA methylation on flowering time in Arabidopsis thaliana. Planta 216: 461-466.
• Grossniklaus U. 2001. From sexuality to apomixis: molecular and genetic approaches. In: Savidan Y, Carman JG, and Dresselhaus T [eds.], The flowering of apomixis: From mechanisms to genetic engineering, 168-211. Mexico, CIMMYT, IRS, Eur. Comm. DG VI.
• Grossniklaus U, Spillane C, Page DR, and Köhler C. 2001. Genomic imprinting and seed development: endosperm formation with and without sex. Current Opinion in Plant Biology 4: 21-27.
• Grossniklaus U, and Schneitz K. 1998. The molecular and genetic basis of ovule and megagametophyte development. Seminars in Cell and Developmental Biology 9: 227-238.
• Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, and Gagliano WB. 1998. Maternal control of embryogenesis by medea, a Polycomb group gene in Arabidopsis. Science 280(5362): 446-450.
• Guitton A, Page D, Chambrier P, Lionnet C, Faure J, Grossniklaus U, and Berger F. 2004. Identification of new members of Fertilisation Independent Seed Polycomb Group pathway involved in the control os seed development in Arabidopsis thaliana. Development 131: 2971-2981.
• Haig D, and Westoby M. 1991. Genomic imprinting in endosperm - Its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 333(1266): 1-13.
• Hashida S, Kitamura K, Mikami T, and Kishima Y. 2003. Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 Antirrhinum majus. Plant Physiology 132: 1207-1216.
• He YM, Michaels SD, and Amasino RM. 2003. Regulation of flowering time by histone acetylation in Arabidopsis. Science 302: 1751-1754.
• Henikoff S, and Comai L. 1998. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307-318.
• Jackson JP, Johnson L, Jasencakova Z, Zhang X, Perezburgos L, Singh PB, Cheng X, Schubert I, Jenuwein T, and Jacobsen SE. 2004. Demethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308-315.
• Jacobsen SE, and Meyerowitz EM. 1997. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100-1103.
• Jeddeloh JA, Bender J, and Richards EJ. 1998. The DNA methylation locus DDM1 is required for maintenance of gene silencing in Arabidopsis. Genes and Development 12: 1714-1725.
• Jeddeloh JA, Stokes TL, and Richards EJ. 1999. Maintenance of genomic methylation requires a SW12/SNF2-like protein. Nature Genetics 22: 94-97.
• Jenuwein T, and Allis CD. 2001. Translating the histone code. Science 293: 1074-1080.
• Johnson L, Cao X, and Jacobsen S. 2002. Interplay between two epigenetic marks: DNA methylation and histone H3 lysine 9 methylation. Current Biology 12: 1360-1367.
• Jones PA, and Takai D. 2001. The role of DNA methylation in mammalian epigenetics. Science 293: 1068-1070.
• Kashkush K, Feldman M, and Levy A. 2003. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genetics 33: 102-106.
• Kinoshita T, Harada JJ, Goldberg RB, and Fischer RL. 2001. Polycomb repression of flowering during early plant development. Proceedings of the National Academy of Sciences of the U.S.A. 98: 14156-14161.
• Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, and Kakutani T. 2004. One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303: 521-523.
• Kinoshita T, Yadegari R, Harada JJ, Goldberg RB, and Fischer RL. 1999. Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11: 1945-1952.
• Köhler C, Henning L, Bouveret R, Gheyselinck J, Grossniklaus U, and Gruissem W. 2003a. Arabidopsis MSI1 is a component of the MEA/FIE polycomb group complex and required for seed development. The EMBO Journal 22: 4804-4814.
• Köhler C, Henning L, Spillane C, Pien S, Gruissem W, and Grossniklaus U. 2003b. The polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes and Development 17: 1540-1553.
• Köhler C, Page DR, Gagliardini V, and Grossniklaus U. 2005. The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nature Genetics 37: 28-30.
• Koltunow AM, Johnson SD, and Bicknell RA. 1998. Sexual and apomictic development in Hieracium. Sexual Plant Reproduction 11: 213-230.
• Koltunow AM, Johnson SD, and Bicknell RA. 2000. Apomixis is not developmentally conserved in related, genetically characterized Hieracium plants of varying ploidy. Sexual Plant Reproduction 12: 253-266.
• Koltunow AMG, and Grossniklaus U. 2003. Apomixis: a developmental perspective. Annual Review of Plant Biology 54: 547-574.
• Labombarda P, Busti A, Caceres M, Pupilli F, and Arcioni S. 2002. An AFLP marker tightly linked to apomixis reveals hemizygosity in a portion of the poamixis-controlling locus in Paspalum simplex. Genome 45: 513-519.
• Lagace M, Chantha S, Major G, and Matton DP. 2003. Fertilization induces strong accumulation of a histone deacetylase (HD2) and of the other chromatin-remodeling proteins in restricted areas of the ovules. Plant Molecular Biology 53: 759-769.
• Lindroth A, Shultis D, Jasencakova Z, Fuchs J, Johnson L, Schubert D, Patnaik D, Pradhan S, Goodrich J, Schubert I, Jenuwein T, Khorasanizadeh S, and Jacobsen SE. 2004. Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. The EMBO Journal 3: 4286-4296.
• Lippman Z, Gendrel A, Black M, Vaugn M, Dedhia N, McComble R, Lavine K, Mittal V, May B, Kasschau K, Carrington J, Doerge R, Colot V, and Martienssen R. 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471-476.
• Luo M, Bilodeau P, Dennis ES, Peacock WJ, and Chaudhury A. 2000. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proceedings of the National Academy of Sciences of the U.S.A. 97: 10637-10642.
• Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, and Chaudhury AM. 1999. Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the U.S.A. 96: 296-301.
• Matzke MA, Mette MF, Aufsatz W, Jakowitsch J, and Matzke AJM. 1999. Host defenses to parasitic sequences and the evolution of epigenetic control mechanism. Genetica 107: 271-287.
• Moon Y, Chen L, Pan R, Chang H, Zhu T, Maffeo D, and Sung Z. 2003. EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. The Plant Cell 15: 681-693.
• Morel J, Mourrain P, Beclin C, and Vaucheret H. 2000. DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Current Biology 10: 1591-1594.
• Mosquna A, Katz A, Shochat S, Grafi G, and Ohad N. 2004. Interaction of FIE, a Polycomb protein, with pRb: a possible mechanism regulating endosperm development. Molecular Genetics and Genomics 271: 651-657.
• Nan X, Ng H, Johnson C, Laherty C, Turner B, Elsenman R, and Bird A. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-389.
• Nogler G. 1984. Gametophytic apomixis. In: Johri BM [ed.], Embryology of Angiosperms, 475-518. Springer-Verlag, Berlin Heidelberg.
• Ohad N, Margossian L, Hsu YC, Williams C, Repetti P, and Fischer RL. 1996. A mutation that allows endosperm development without fertilization. Proceedings of the National Academy of Sciences of the U.S.A. 93: 5319-5324.
• Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB, and Fischer RL. 1999. Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11: 407-415.
• Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, Bender J, Mount DW, and Jorgensen RA. 2002. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Research 30: 5036-5055.
• Pasini D, Bracken A, and Helin K. 2004. Polycomb Group Proteins in cell cycle progression and cancer. Cell Cycle 3: 396-400.
• Peaston A, Evsikov A, Graber J, De Vries W, Holbrook A, Solter D, and Knowles B. 2004. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Developmental Cell 7: 597-606.
• Pirrota V, Poux S, Melfi R, and Pilyugin M. 2003. Assembly of polycomb complexes and silencing mechanisms. Genetica 117: 191-197.
• Robertson K, Ait-Si-Ali S, Yokochi T, Wade P, Jones P, and Wolffe A. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nature Genetics 25: 338-342.
• Ronemus MJ, Galbiati M, Ticknor C, Chen J, and Dellaporta SL. 1996. Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273: 654-657.
• Sakai H, Medrano LJ, and Meyerowitz EM. 1995. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378: 199-203.
• Savidan Y. 2000. Apomixis, the way of cloning seeds. Biofutur 2000(198): 38-43.
• Saze H, Scheid OM, and Paszkowski J. 2003. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nature Genetics 34: 65-69.
• Schramke V, and Allshire R. 2003. Hairpin RNAs and retrotransposon LTRs effect RNAi and chromatin-based gene silencing. Science 301: 1069-1074.
• Simon J, and Tamkun J. 2002. Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes. Current Opinion in Genetics and Development 12: 210-218.
• Soppe WJJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, and Peeters AJM. 2000. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Molecular Cell 6: 791-802.
• Spillane C, MacDougall C, Stock C, Köhler C, Vielle-Calzada JP, Nunes SM, Grossniklaus U, and Goodrich J. 2000. Interaction of the Arabidopsis Polycomb group proteins FIE and MEA mediates their common phenotypes. Current Biology 10: 1535-1538.
• Steimer A, Schob H, and Grossniklaus U. 2004. Epigenetic control of plant development: new layers of complexity. Current Opinion in Plant Biology 7: 11-19.
• Strahl BD, and Allis CD. 2000. The language of covalent histone modifications. Nature 403: 41-45.
• Sung S, and Amasino RM. 2004. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159-164.
• Tian L, and Chen ZJ. 2001. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proceedings of the National Academy of Sciences of the U.S.A. 98: 200-205.
• Tie F, Furuyama T, Prasad-Sinha J, Jane E, and Harte PJ. 2001. The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deacetylase RPD3. Development 128: 275-286.
• Tucker MR, Araujo AG, Paech NA, Hecht V, Schimidt EDL, Rossel J, Vries SC, and Koltunow AMG. 2003. Sexual and apomictic reproduction in Hieracium subgenus pilosella are closely interrelated developmental pathways. Plant Cell 15: 1524-1537.
• Vielle-Calzada JP, Baskar R, and Grossniklaus U. 2000. Delayed activation of the paternal genome during seed development. Nature 404(6773): 91-94.
• Vielle-Calzada JP, Thomas J, Spillane C, Coluccio A, Hoeppner MA, and Grossniklaus U. 1999. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes and Development 13: 2971-2982.
• Vinkenoog R, and Scott RJ. 2001. Autonomous endosperm development in flowering plants: how to overcome the imprinting problem? Sexual Plant Reproduction 14: 189-194.
• Vinkenoog R, Spielman M, Adams S, Fischer RL, Dickinson HG, and Scott RJ. 2000. Hypomethylation promotes autonomous endosperm development and rescues postfertilization lethality in fie mutants. Plant Cell 12: 2271-2282.
• Walsh CP, and Bestor TH. 1999. Cytosine methylation and mammalian development. Genes and Development 13: 26-34.
• Wu KQ, Tian LN, Malik K, Brown D, and Miki B. 2000. Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana. Plant Journal 22: 19-27.
• Xiao W, Gehring M, Choi Y, Margossian L, Pu H, Harada JJ, Goldberg RB, Pennell RI, and Fischer RL. 2003. Imprinting of the MEA polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Developmental Cell 5: 891-901.
• Yoshida N, Yanai Y, Chen LJ, Kato Y, Hiratsuka J, Miwa T, Sung ZR, and Takahashi S. 2001. EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13: 2471-2481.
• Zhou C, Labbe H, Sridha S, Wang L, Tian L, Latoszek-Green M, Yang Z, Brown D, Miki B, and Wu K. 2004. Expression and function of HD2-type histone deacetylases in Arabidopsis development. The Plant Journal 38: 715-724.