Polycomb Group Gene OsFIE2 Regulates Rice (Oryza sativa) Seed Development and Grain Filling via a Mechanism Distinct from Arabidopsis

PLoS Genetics

Volumn 9, Issue 3, 2013, Pages

  Nallamilli, Babi Ramesh Reddy ^a   Zhang, Jian ^a   Mujahid, Hana ^a   Malone, Brandon M ^a,b   Bridges, Susan M ^a,b   Peng, Zhaohua ^a  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELIX LOOP HELIX PROTEIN; POLYCOMB GROUP PROTEIN;

ARABIDOPSIS; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DOWN REGULATION; ENDOSPERM; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC REGULATION; GENOME ANALYSIS; GRAIN FILLING; HISTONE MODIFICATION; NONHUMAN; OSFIE2 GENE; PHENOTYPE; PLANT GENE; PROTEIN DNA BINDING; PROTEIN INTERACTION; PROTEOMICS; RICE; SEED DEVELOPMENT; SEED DORMANCY; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CEREALS; GENE EXPRESSION REGULATION, PLANT; HISTONE-LYSINE N-METHYLTRANSFERASE; MULTIPROTEIN COMPLEXES; ORYZA SATIVA; POLYCOMB-GROUP PROTEINS; REPRESSOR PROTEINS; SEED DORMANCY; SEEDS;

ARABIDOPSIS; ORYZA SATIVA;

EID: 84875994393     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003322     Document Type: Article

References (91)

1. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G, (2007) Genome regulation by polycomb and trithorax proteins. Cell 128: 735-745.
2. Schwartz YB, Pirrotta V, (2008) Polycomb complexes and epigenetic states. Curr Opin Cell Biol 20: 266-273.
3. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C, (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A 105: 16831-16836.
4. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, et al. (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44-51.
5. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB, (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280: 446-450.
6. Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, et al. (1999) Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11: 407-416.
7. Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, et al. (1999) Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 96: 296-301.
8. Kohler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, et al. (2003a) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J 22: 4804-4814.
9. Kohler C, Hennig L, Spillane C, Pien S, Gruissem W, et al. (2003b) The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17: 1540-1553.
10. Huh JH, Bauer MJ, Hsieh TF, Fischer RL, (2008) Cellular programming of plant gene imprinting. Cell 132: 735-744.
11. Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, et al. (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263-5276.
12. Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A, (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci U S A 97: 10637-10642.
13. Katz A, Oliva M, Mosquna A, Hakim O, Ohad N, (2004) FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37: 707-719.
14. Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, et al. (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci U S A 103: 14631-14636.
15. Spillane C, MacDougall C, Stock C, Kohler C, Vielle-Calzada JP, et al. (2000) Interaction of the Arabidopsis polycomb group proteins FIE and MEA mediates their common phenotypes. Curr Biol 10: 1535-1538.
16. Yadegari R, Kinoshita T, Lotan O, Cohen G, Katz A, et al. (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.
17. Wang D, Tyson MD, Jackson SS, Yadegari R, (2006) Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in Arabidopsis. Proc Natl Acad Sci U S A 103: 13244-13249.
18. Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, et al. (2001) EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13: 2471-2481.
19. Jiang H, Wong WH, (2008) SeqMap: mapping massive amount of oligonucleotides to the genome. Bioinformatics 24: 2395-2396.
20. Schonrock N, Bouveret R, Leroy O, Borghi L, Kohler C, et al. (2006) Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev 20: 1667-1678.
21. Gendall AR, Levy YY, Wilson A, Dean C, (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107: 525-535.
22. Sung S, Amasino RM, (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159-164.
23. Angel A, Song J, Dean C, Howard M, (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476: 105-108.
24. Nowack MK, Shirzadi R, Dissmeyer N, Dolf A, Endl E, et al. (2007) Bypassing genomic imprinting allows seed development. Nature 447: 312-315.
25. Gehring M, Choi Y, Fischer RL, (2004) Imprinting and seed development. Plant Cell 16 Suppl: S203-213.
26. Guitton AE, Page DR, Chambrier P, Lionnet C, Faure JE, et al. (2004) Identification of new members of Fertilisation Independent Seed Polycomb Group pathway involved in the control of seed development in Arabidopsis thaliana. Development 131: 2971-2981.
27. Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, et al. (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 94: 4223-4228.
28. Kiyosue T, Ohad N, Yadegari R, Hannon M, Dinneny J, et al. (1999) Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc Natl Acad Sci U S A 96: 4186-4191.
29. Xiao W, Gehring M, Choi Y, Margossian L, Pu H, et al. (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5: 891-901.
30. Leroy O, Hennig L, Breuninger H, Laux T, Kohler C, (2007) Polycomb group proteins function in the female gametophyte to determine seed development in plants. Development 134: 3639-3648.
31. Kinoshita T, Yadegari R, Harada JJ, Goldberg RB, Fischer RL, (1999) Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11: 1945-1952.
32. Jullien PE, Katz A, Oliva M, Ohad N, Berger F, (2006a) Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol 16: 486-492.
33. Jullien PE, Kinoshita T, Ohad N, Berger F, (2006b) Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18: 1360-1372.
34. Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, et al. (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7: e1002014 doi:10.1371/journal.pgen.1002014.
35. Roszak P, Kohler C, (2011) Polycomb group proteins are required to couple seed coat initiation to fertilization. Proc Natl Acad Sci U S A 108: 20826-20831.
36. Danilevskaya ON, Hermon P, Hantke S, Muszynski MG, Kollipara K, et al. (2003) Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15: 425-438.
37. Gutierrez-Marcos JF, Costa LM, Dal Pra M, Scholten S, Kranz E, et al. (2006) Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet 38: 876-878.
38. Hermon P, Srilunchang KO, Zou J, Dresselhaus T, Danilevskaya ON, (2007) Activation of the imprinted Polycomb Group Fie1 gene in maize endosperm requires demethylation of the maternal allele. Plant Mol Biol 64: 387-395.
39. Springer NM, Danilevskaya ON, Hermon P, Helentjaris TG, Phillips RL, et al. (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.
40. Haun WJ, Laoueille-Duprat S, O'Connell M J, Spillane C, Grossniklaus U, et al. (2007) Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J 49: 325-337.
41. Kapazoglou A, Tondelli A, Papaefthimiou D, Ampatzidou H, Francia E, et al. (2010) Epigenetic chromatin modifiers in barley: IV. The study of barley polycomb group (PcG) genes during seed development and in response to external ABA. BMC Plant Biol 10: 73.
42. Luo M, Platten D, Chaudhury A, Peacock WJ, Dennis ES, (2009) Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2: 711-723.
43. Liang YK, Wang Y, Zhang Y, Li SG, Lu XC, et al. (2003) OsSET1, a novel SET-domain-containing gene from rice. J Exp Bot 54: 1995-1996.
44. Thakur JK, Malik MR, Bhatt V, Reddy MK, Sopory SK, et al. (2003) A POLYCOMB group gene of rice (Oryza sativa L. subspecies indica), OsiEZ1, codes for a nuclear-localized protein expressed preferentially in young seedlings and during reproductive development. Gene 314: 1-13.
45. Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, et al. (2011) A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet 7: e1002125 doi:10.1371/journal.pgen.1002125.
46. Rodrigues JC, Luo M, Berger F, Koltunow AM, (2010) Polycomb group gene function in sexual and asexual seed development in angiosperms. Sex Plant Reprod 23: 123-133.
47. Spillane C, Schmid KJ, Laoueille-Duprat S, Pien S, Escobar-Restrepo JM, et al. (2007) Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448: 349-352.
48. Rodrigues JC, Tucker MR, Johnson SD, Hrmova M, Koltunow AM, (2008) Sexual and apomictic seed formation in Hieracium requires the plant polycomb-group gene FERTILIZATION INDEPENDENT ENDOSPERM. Plant Cell 20: 2372-2386.
49. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, et al. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030-1032.
50. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, et al. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229.
51. Rohila JS, Chen M, Cerny R, Fromm ME, (2004) Improved tandem affinity purification tag and methods for isolation of protein heterocomplexes from plants. Plant J 38: 172-181.
52. Rubio V, Shen Y, Saijo Y, Liu Y, Gusmaroli G, et al. (2005) An alternative tandem affinity purification strategy applied to Arabidopsis protein complex isolation. Plant J 41: 767-778.
53. Rohila JS, Chen M, Chen S, Chen J, Cerny R, et al. (2006) Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice. Plant J 46: 1-13.
54. Van Leene J, Stals H, Eeckhout D, Persiau G, Van De Slijke E, et al. (2007) A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol Cell Proteomics 6: 1226-1238.
55. Brown AP, Affleck V, Fawcett T, Slabas AR, (2006) Tandem affinity purification tagging of fatty acid biosynthetic enzymes in Synechocystis sp. PCC6803 and Arabidopsis thaliana. J Exp Bot 57: 1563-1571.
56. Rivas S, Romeis T, Jones JD, (2002) The Cf-9 disease resistance protein is present in an approximately 420-kilodalton heteromultimeric membrane-associated complex at one molecule per complex. Plant Cell 14: 689-702.
57. Abe M, Fujiwara M, Kurotani K, Yokoi S, Shimamoto K, (2008) Identification of dynamin as an interactor of rice GIGANTEA by tandem affinity purification (TAP). Plant Cell Physiol 49: 420-432.
58. Chitteti BR, Tan F, Mujahid H, Magee BG, Bridges SM, et al. (2008) Comparative analysis of proteome differential regulation during cell dedifferentiation in Arabidopsis. Proteomics 8: 4303-4316.
59. Tan F, Li G, Chitteti BR, Peng Z, (2007) Proteome and phosphoproteome analysis of chromatin associated proteins in rice (Oryza sativa). Proteomics 7: 4511-4527.
60. Tan F, Zhang K, Mujahid H, Verma DP, Peng Z, (2010) Differential histone modification and protein expression associated with cell wall removal and regeneration in rice (Oryza sativa). J Proteome Res 10: 551-563.
61. Tie F, Stratton CA, Kurzhals RL, Harte PJ, (2007) The N terminus of Drosophila ESC binds directly to histone H3 and is required for E(Z)-dependent trimethylation of H3 lysine 27. Mol Cell Biol 27: 2014-2026.
62. Verreault A, Kaufman PD, Kobayashi R, Stillman B, (1998) Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr Biol 8: 96-108.
63. Vermaak D, Wade PA, Jones PL, Shi YB, Wolffe AP, (1999) Functional analysis of the SIN3-histone deacetylase RPD3-RbAp48-histone H4 connection in the Xenopus oocyte. Mol Cell Biol 19: 5847-5860.
64. Joung JK, Ramm EI, Pabo CO, (2000) A bacterial two-hybrid selection system for studying protein-DNA and protein-protein interactions. Proc Natl Acad Sci U S A 97: 7382-7387.
65. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043.
66. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, et al. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196.
67. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D, (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905.
68. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208.
69. Ohdan T, Francisco PB Jr, Sawada T, Hirose T, Terao T, et al. (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 56: 3229-3244.
70. Giroux MJ, Boyer C, Feix G, Hannah LC, (1994) Coordinated Transcriptional Regulation of Storage Product Genes in the Maize Endosperm. Plant Physiol 106: 713-722.
71. She KC, Kusano H, Koizumi K, Yamakawa H, Hakata M, et al. (2010) A novel factor FLOURY ENDOSPERM2 is involved in regulation of rice grain size and starch quality. Plant Cell 22: 3280-3294.
72. Li G, Nallamilli BR, Tan F, Peng Z, (2008) Removal of high-abundance proteins for nuclear subproteome studies in rice (Oryza sativa) endosperm. Electrophoresis 29: 604-617.
73. Malone BM, Tan F, Bridges SM, Peng Z, (2011) Comparison of four ChIP-Seq analytical algorithms using rice endosperm H3K27 trimethylation profiling data. PLoS ONE 6: e25260 doi:10.1371/journal.pone.0025260.
74. Egelhofer TA, Minoda A, Klugman S, Lee K, Kolasinska-Zwierz P, et al. (2011) An assessment of histone-modification antibody quality. Nat Struct Mol Biol 18: 91-93.
75. Kondou Y, Nakazawa M, Kawashima M, Ichikawa T, Yoshizumi T, et al. (2008) Retarded growth of EMBRYO1, a new basic helix-loop-helix protein, expression in endosperm to control embryo growth. Plant Physiol 147: 1924-1935.
76. Yang S, Johnston N, Talideh E, Mitchell S, Jeffree C, et al. (2008) The endosperm-specific ZHOUPI gene of Arabidopsis thaliana regulates endosperm breakdown and embryonic epidermal development. Development 135: 3501-3509.
77. Swiezewski S, Liu F, Magusin A, Dean C, (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462: 799-802.
78. Heo JB, Sung S, (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79.
79. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, et al. (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164-167.
80. Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, et al. (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124: 495-506.
81. Zhang J, Nallamilli BR, Mujahid H, Peng Z, (2010) OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J 64: 604-617.
82. Wu C, Li X, Yuan W, Chen G, Kilian A, et al. (2003) Development of enhancer trap lines for functional analysis of the rice genome. Plant J 35: 418-427.
83. Miki D, Shimamoto K, (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45: 490-495.
84. Li J, Moazed D, Gygi SP, (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J Biol Chem 277: 49383-49388.
85. Chitteti BR, Peng Z, (2007) Proteome and phosphoproteome dynamic change during cell dedifferentiation in Arabidopsis. Proteomics 7: 1473-1500.
86. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
87. Chhun T, Aya K, Asano K, Yamamoto E, Morinaka Y, et al. (2007) Gibberellin regulates pollen viability and pollen tube growth in rice. Plant Cell 19: 3876-3888.
88. Gendrel AV, Lippman Z, Martienssen R, Colot V, (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2: 213-218.
89. Jiang H, Wong WH, (2008) SeqMap: mapping massive amount of oligonucleotides to the genome. Bioinformatics 24: 2395-2396.
90. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, et al. (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35: D883-887.
91. Fejes AP, Robertson G, Bilenky M, Varhol R, Bainbridge M, et al. (2008) FindPeaks 3.1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology. Bioinformatics 24: 1729-1730.