Chromatin and DNA modifications in the opaque2-mediated regulation of gene transcription during maize endosperm development

Plant Cell

Volumn 21, Issue 5, 2009, Pages 1410-1427

  Locatelli, Sabrina ^a   Piatti, Paolo ^a   Motto, Mario ^b   Rossi, Vincenzo ^b  

^a ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ZEA MAYS;

EID: 67651121609     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.067256     Document Type: Article

References (71)

1. Agalioti, T., Chen, G., and Thanos, D. (2002). Deciphering the tran-scriptional histone acetylation code for a human gene. Cell 111: 381-392. (Pubitemid 35341391)
2. Ahmad, K., and Henikoff, S. (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9: 1191-1200. (Pubitemid 34722299)
3. Baroux, C., Pecinka, A., Fuchs, J., Schubert, I., and Grossniklaus, U. (2007). The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell 19: 1782-1794. (Pubitemid 47218840)
4. Berger, S.L. (2007). The complex language of chromatin regulation during transcription. Nature 447: 407-412. (Pubitemid 46816746)
5. Bhat, R.A., Borst, J.W., Riehl, M., and Thompson, R.D. (2004). Interaction of maize Opaque-2 and the transcriptional co-activators GCN5 and ADA2, in the modulation of transcriptional activity. Plant Mol. Biol. 55: 239-252.
6. Bhat, R.A., Riehl, M., Santandrea, G., Velasco, R., Slocombe, S., Donn, G., Steinbiss, H.H., Thompson, R.D., and Becker, H.A. (2003). Alteration of GCN5 levels in maize reveals dynamic responses to manipulating histone acetylation. Plant J. 33: 455-470. (Pubitemid 36257459)
7. Boss, P.K., Bastow, R.M., Mylne, J.S., and Dean, C. (2004). Multiple pathways in the decision to flower: Enabling, promoting, and resetting. Plant Cell 16(Suppl.): S18-S31. (Pubitemid 38774214)
8. Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M., and Jacobsen, S.E. (2008). Shotgun bisulphite sequencing of the Arabi-dopsis reveals DNA methylation patterning. Nature 452: 215-219.
9. Danker, T., Dreesen, B., Offermann, S., Horst, I., and Peterhansel, C. (2008). Developmental information but not promoter activity controls the methylation state of histone H3 lysine 4 on two photosynthetic genes in maize. Plant J. 53: 465-474. (Pubitemid 351172016)
10. Fry, C.Y., and Peterson, C.L. (2001). Chromatin remodeling enzymes: Who's on first. Curr. Biol. 11: R185-R197.
11. Gallusci, P., Salamini, F., and Thompson, R.D. (1994). Differences in cell typespecific expression of the gene Opaque 2 in maize and transgenic tobacco. Mol. Gen. Genet. 244: 391-400. (Pubitemid 24266098)
12. Gallusci, P., Varotto, S., Matsuoko, M., Maddaloni, M., and Thompson, R.D. (1996). Regulation of pyruvate, orthophosphate dikinase expression in maize endosperm. Plant Mol. Biol. 31: 45-55.
13. Goldberg, A.D., Allis, C.D., and Bernstein, E. (2007). Epigenetics: A landscape takes shape. Cell 128: 635-638. (Pubitemid 46273578)
14. Gutierrez-Marcos, J.F., Costa, L.M., Scholten, S., dal Pra, M., Perez, P., Kranz, E., and Dickinson, H.G. (2006). Different epigenetic marks regulate imprinting in maize. Nat. Genet. 38: 876-878.
15. Hartings, H., Lazzaroni, N., Rossi, V., Riboldi, G.R., Thompson, R.D., Salamini, F., and Motto, M. (1995). Molecular analysis of opaque-2 alleles from Zea mays L. reveals the nature of mutational events and the presence of a hypervariable region in the 59 part of the gene. Genet. Res. 65: 11-19.
16. Hartings, H., Maddaloni, M., Lazzaroni, N., Di Fonzo, N., Motto, M., Salamini, F., and Thompson, R.D. (1989). The O2 gene which regulates zein deposition in maize endosperm encodes a protein with structural homologies to transcriptional activators. EMBO J. 8: 2795-2801.
17. He, Y., Doyle, M.R., and Amasino, R.M. (2004). PAF1-complexmedi-ated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18: 2774-2784. (Pubitemid 39507770)
18. Hunter, B.G., Beatty, M.K., Singletary, G.W., Hamaker, B.R., Dilkes, B.P., Larkins, B.A., and Jung, R. (2002). Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14: 2591-2612. (Pubitemid 35224852)
19. Jacobsen, S.E., Sakai, H., Finnegan, E.J., Cao, X., and Meyerowitz, E.M. (2000). Ectopic methylation of flower-specific genes in Arabi-dopsis. Curr. Biol. 10: 179-186. (Pubitemid 30146782)
20. Kemper, E.L., Neto, G.C., Papes, F., Moraes, K.C.M., Leite, A., and Arruda, P. (1999). The role of Opaque2 in the control of lysine degrading activities in developing maize endosperm. Plant Cell 11: 1981-1993.
21. Kertesz, S., Kerenyi, Z., Merai, Z., Bartos, I., Palfy, T., Barta, E., and Silhavy, D. (2006). Both introns and 39-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucleic Acids Res. 34: 6147-6157. (Pubitemid 44942736)
22. Kodrzycki, R., Boston, R.S., and Larkins, B.A. (1989). The opaque-2 mutation of maize differentially reduces zein gene transcription. Plant Cell 1: 105-114.
23. Kouzarides, T. (2007). Chromatin modifications and their functions. Cell 128: 693-705.
24. Krogan, N.J., Dover, J., Wood, A., Schneider, J., Heidt, J., Boateng, M.A., Dean, K., Ryan, O.W., Golshani, A., Johnston, M., Greenblatt, J.F., and Shilatifard, A. (2003). The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongationtohistone methylation. Mol. Cell11: 721-729. (Pubitemid 36385125)
25. Lauria, M., Rupe, M., Guo, M., Pirona, R., Viotti, A., and Lund, G. (2004). Extensive maternal DNA hypomethylation in the endosperm of Zea mays. Plant Cell 16: 510-522. (Pubitemid 38192706)
26. Li, B., Carey, M., and Workman, J.L. (2007). The role of chromatin during transcription. Cell 128: 707-709. (Pubitemid 46273570)
27. Li, G., Chandrasekharan, M.B., Wolffe, A.P., and Hall, T.C. (2001). Chromatin structure and phaseolin gene regulation. Plant Mol. Biol. 46: 121-129. (Pubitemid 32595969)
28. Li, G., Hall, T.C., and Holmes-Davis, R. (2002). Plant chromatin: Development and gene control. Bioessays 24: 234-243. (Pubitemid 34248689)
29. Li, X., et al. (2008). High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20: 259-276. (Pubitemid 352844011)
30. Liu, C.L., Kaplan, T., Kim, M., Buratowski, S., Schreiber, S.L., Friedman, N., and Rando, O.J. (2005). Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3: e328. (Pubitemid 41437148)
31. Liu, C.N., and Rubenstein, I. (1993). Transcriptional characterization of an a-zein gene cluster in maize. Plant Mol. Biol. 2: 323-336.
32. Lohmer, S., Maddaloni, M., Motto, M., Di Fonzo, N., Hartings, H., Salamini, F., and Thompson, R.D. (1991). The maize regulatory locus opaque-2 encodes a DNA-binding protein which activates transcription of the b-32 gene. EMBO J. 10: 617-624. (Pubitemid 21905515)
33. Loyola, A., and Almouzni, G. (2007). Marking histone H3 variants: How, when, and why? Trends Biochem. Sci. 32: 425-433. (Pubitemid 47369165)
34. Lund, G., Ciceri, P., and Viotti, A. (1995a). Maternal-specific demeth-ylation and expression of specific alleles of zein genes in the endosperm of Zea mays L. Plant J. 8: 571-581.
35. Lund, G., Das, O.P., and Messing, J. (1995b). Tissue-specific DNAse I-sensitive sites of the maize P gene and their changes upon epimutation. Plant J. 7: 797-807.
36. Luthe, D.S., and Quatrano, R.S. (1980). Transcription in isolated wheat nuclei. Plant Physiol. 65: 305-308.
37. Maddaloni, M., Donini, G., Balconi, C., Rizzi, E., Gallusci, P., Forlani, F., Lohmer, S., Thompson, R.D., Salamini, F., and Motto, M. (1996). The transcriptional activator Opaque-2 controls the expression of cytosolic form of pyruvate orthophosphate dikinase-1 in maize endosperms. Mol. Gen. Genet. 250: 647-654. (Pubitemid 126451409)
38. Mauri, I., Maddaloni, M., Lohmer, S., Motto, M., Salamini, F., Thompson, R.D., and Martegani, E. (1993). Functional expression of the transcriptional activator Opaque-2 of Zea mays in transformed yeast. Mol. Gen. Genet. 241: 319-326. (Pubitemid 23330662)
39. McArthur, M., Gerum, S., and Stamatoyannopoulos, G. (2001). Quantification of DNAseI-sensitivity by real-time PCR: Quantitative analysis of DNAseI hypersensitivity of the mouse b-globin LCR. J. Mol. Biol. 313: 27-34. (Pubitemid 33001163)
40. Muth, J.R., Muller, S., Lohmer, S., Salamini, F., and Thompson, R.D. (1996). The role of multiple binding sites in the activation of zein gene expression by Opaque-2. Mol. Gen. Genet. 252: 723-732. (Pubitemid 26378985)
41. Ng, D.W.-K., Chandrasekharan, M.B., and Hall, T.C. (2006). Ordered histone modifications are associated with the transcriptional poising and activation of the phaseolin promoter. Plant Cell 18: 119-132.
42. Offermann, S., Dreesen, B., Horst, I., Danker, T., Jaskiewicz, M., and Peterhansel, C. (2008). Developmental and environmental signals induce distinct histone acetylation profiles on distal and proximal promoter elements of the C4-Pepc gene in maize. Genetics 179: 1891-1901.
43. Pien, S., Fleury, D., Mylne, J.S., Crevillen, P., Inzé, D., Avramova, Z., Dean, C., and Grossniklaus, U. (2008). ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trymethylation. Plant Cell 20: 580-588. (Pubitemid 352843994)
44. Pirona, R., Hartings, H., Lauria, M., Rossi, V., and Motto, M. (2005). Genetic control of endosperm development and of storage products accumulation on maize seeds. Maydica 50: 515-530.
45. Plotnikov, V.K., and Bakaldina, N.B. (1996). Differential stability of zein mRNA in developing corn kernel. Plant Mol. Biol. 31: 507-515.
46. Pysh, L.D., Aukerman, L.J., and Schmidt, R.J. (1993). OHP1: A maizebasic domain/leucine zipper protein that interacts with Opaque2. Plant Cell 5: 227-236.
47. Rossi, V., Locatelli, S., Varotto, S., Donn, G., Pirona, R., Henderson, D.A., Hartings, H., and Motto, M. (2007). Maize histone deacetylase hda101 is involved in plant development, gene transcription, and sequence-specific modulation of histone modification of genes and repeats. Plant Cell 19: 1145-1162. (Pubitemid 46941645)
48. Rossi, V., Motto, M., and Pellegrini, L. (1997). Analysis of the meth-ylation pattern of the maize opaque-2 (O2) promoter and in vitro binding studies indicate that the O2 bZIP protein and other endosperm factors can bind to methylated target sequences. J. Biol. Chem. 272: 13758-13765. (Pubitemid 27224813)
49. Saleh, A., Al-Abdallat, A., Namukong, I., Alvarez-Vanegas, R., and Avramova, Z. (2007). The Arabidopsis homologs of trithorax (ATX1) of Enhancer of zeste establish 'bivalent chromatin marks' at the silent AGAMOUS locus. Nucleic Acids Res. 35: 6290-6296. (Pubitemid 350018590)
50. Sano, Y., and Tanaka, I. (2007). Detection of differentially expressed variant histone H3.3 in vegetative nucleus of lily pollen. Sex. Plant Reprod. 20: 27-33. (Pubitemid 46309220)
51. Schmidt, R.J., Burr, F.A., Aukerman, M.J., and Burr, B. (1990). Maize regulatory gene opaque-2 encodes a protein with a leucine zipper motif that binds to zein DNA. Proc. Natl. Acad. Sci. USA 87: 46-50. (Pubitemid 20033003)
52. Schmidt, R.J., Burr, F.A., and Burr, B. (1987). Transposon tagging and molecular analysis of the maize regulatory locus opaque-2. Science 238: 960-963.
53. Schmidt, R.J., Ketudat, M., Aukerman, M.J., and Hoschek, G. (1992). Opaque-2 is a transcriptional activator that recognizes a specific target site in 22 kD zein genes. Plant Cell 4: 689-700.
54. Schmitz, R.J., and Amasino, R.M. (2007). Vernalization: A model for investigating epigenetics and eukaryotic gene regulation in plants. Biochim. Biophys. Acta 1769: 269-275.
55. Shah, D.M., Hightower, R.C., and Meagher, R.B. (1983). Genes encoding actin in higher plants: Intron positions are highly conserved but the coding sequences are not. J. Mol. Appl. Genet. 2: 111-126.
56. Sheen, J. (1991). Molecular mechanisms underlying the differential expression of maize pyruvate, orthophospate dikinase genes. Plant Cell 3: 225-245. (Pubitemid 21913692)
57. Spena, A., Viotti, A., and Pirrotta, V. (1983). Two adjacent genomic zein sequences: structure, organization and tissue-specific restriction pattern. J. Mol. Biol. 169: 799-811.
58. Sturaro, M., and Viotti, A. (2001). Methylation of the Opaque2 box inzein genes is parent dependent and affects O2 DNA binding activity, in vitro. Plant Mol. Biol. 46: 549-560. (Pubitemid 32739405)
59. Song, R., Llaca, V., Linton, E., and Messing, J. (2001). Sequence, regulation, and evolution of the maize 22-kD α zein gene family. Genome Res. 11: 1817-1825. (Pubitemid 33100421)
60. Song, R., and Messing, J. (2002). Contiguous genomic DNA sequence comprising the 19-kDa-zein gene family from Zea mays. Plant Physiol. 130: 1626-1635. (Pubitemid 36035163)
61. Song, R., and Messing, J. (2003). Gene expression of a gene family in maize based on non-collinear haplotypes. Proc. Natl. Acad. Sci. USA 100: 9055-9060. (Pubitemid 36899222)
62. Strahl, B.D., and Allis, C.D. (2000). The language of covalent histone modifications. Nature 403: 41-45.
63. Swanson, M.J., Qiu, H., Sumibcay, L., Krueger, A., Kim, S.-J., Natarajan, K., Yoon, S., and Hinnebusch, A.G. (2003). A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo. Mol. Cell. Biol. 23: 2800-2820. (Pubitemid 36403079)
64. Varotto, S., Locatelli, S., Canova, S., Pipal, A., Motto, M., and Rossi, V. (2003). Expression profile and cellular localization of maize Rpd3-type histone deacetylases during plant development. Plant Physiol. 133: 606-617. (Pubitemid 37325673)
65. Vicente-Carbajosa, J., Moose, S.P., Parsons, R.L., and Schmidt, R.J. (1997). A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcrip-tional activator Opaque-2. Proc. Natl. Acad. Sci. USA 94: 7685-7690. (Pubitemid 27345377)
66. Yu, C., Palumbo, M.J., Lawrence, C.E., and Morse, R.H. (2006). Contribution of the histone H3 and H4 amino termini to Gcn4p-and Gcn5p-mediated transcription in yeast. J. Biol. Chem. 14: 9755-9764. (Pubitemid 43864694)
67. Wang, Z., Ueda, T., and Messing, J. (1998). Characterization of the maize prolamine box-binding factor-1 (PBF-1) and its role in the developmental regulation of the zein multigene family. Gene 223: 321-332. (Pubitemid 29015940)
68. Weil, C., and Martienssen, R. (2008). Epigenetic interactions between transposons and genes: Lessons from plants. Curr. Opin. Genet. Dev. 18: 188-192. (Pubitemid 351749827)
69. Wurtzel, E.T., Burr, F.A., and Burr, B. (1987). DNAse I hypersensivity and expression of the Shrunken-1 gene of maize. Plant Mol. Biol. 8: 251-264.
70. Zhang, Y. (2008). The epigenetic landscape of plants. Science 320: 489-492.
71. Zilberman, D., and Henikoff, S. (2007). Genome-wide analysis of DNA methylation patterns. Development 134: 3959-3965. (Pubitemid 350269413)