Overexpression of several Arabidopsis histone genes increases Agrobacterium-mediated transformation and transgene expression in plants

Plant Cell

Volumn 21, Issue 10, 2009, Pages 3350-3367

  Tenea, Gabriela N ^a,b   Spantzel, Joerg ^a   Lee, Lan Ying ^a   Zhu, Yanmin ^a,c   Lin, Kui ^a,d   Johnson, Susan J ^a,e   Gelvin, Stanton B ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF BUCHAREST   (Romania)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d SHANGHAI JIAO TONG UNIVERSITY   (China)

^e MONSANTO COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGROBACTERIUM; AGROBACTERIUM TUMEFACIENS; ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM; RHIZOBIUM;

EID: 72049115218     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.070607     Document Type: Article

References (110)

1. Anand, A., Zarir, V., Ryu, C.M., Kang, L., del-Pozo, O., Martin, G.B., and Mysore, K.S. (2007). Identification of plant genes involved in Agrobacferium-mediated transformation by using virus induced gene silencing as a functional genomics tool. Mol. Plant Microbe Interact. 20: 41-52.
2. Baake, M., Doenecke, D., and Albig, W. (2001). Characterisation of nuclear localisation signals of the four human core histones. J. Cell. Biochem. 81: 333-346.
3. Balicki, D., Putnam, C.D., Scaria, P.V., and Beutler, E. (2002). Structure and function correlation in histone H2A peptide-mediated gene transfer. Proc. Natl. Acad. Sci. USA 99: 7467-7471.
4. Bailas, N., and Citovsky, V. (1997). Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc. Natl. Acad. Sci. USA 94: 10723-10728.
5. Bhattacharjee S, Lee LY, Oltmanns H, Cao H, Veena, Cuperus J, Gelvin SB. (2008). Atlmpa-4, an Arabidopsis importin a isoform, is preferentially involved in Agrobacterium-mediated plant transformation. Plant Cell 20: 2661-2680.
6. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 72: 248-254.
7. Branscombe, T.L., Frankel, A., Lee, J.H., Cook, J.R., Yang, Z., Pestka, S., and Clarke, S. (2001). PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J. Biol. Chem. 276: 32971-32976.
8. Brunaud, V., et al. (2002). T-DNA Integration into the Arabidopsis genome depends on sequences of pre-insertion sites. EMBO Rep. 3: 1152-1157.
9. Carruthers, L., and Hansen, J.C. (2000). The core histone N termini function independently of linker histones during chromatin condensation. J. Biol. Chem. 275: 37285-37290.
10. Chan, S.W., Henderson, I.R., and Jacobsen, S.E. (2007). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet. 6: 351-360.
11. Christie, P.J., Ward, J.E., Winans, S.C., and Nester, E.W. (1988). The Agrobacterium tumefaciens virE2 gene product is a single-stranded DNA-binding protein that associates with T-DNA. J. Bacteriol. 170: 2659-2667.
12. Citovsky, V., De Vos, G., and Zambryski, P. (1988). Single-stranded DNA binding protein encoded by the virE locus of Agrobacterium tumefaciens. Science 240: 501-504.
13. Citovsky, V., Kozlovsky, S.V., Lacroix, B., Zaltsman, A., Dafny-Yelin, M., Vyas, S., Tovkach, A., and Tzfira, T. (2007). Biological systems of the host cell involved in Agrobacterium infection. Cell. Microbiol. 9: 9-20.
14. Citovsky, V., Lee, L.-Y., Vyas, S., Glick, E., Chen, M.-H., Vainstein, A., Gafni, Y., Gelvin, S.B., and Tzfira, T. (2006). Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J. Mol. Biol. 362: 1120-1131. (Pubitemid 44353530)
15. Citovsky, V., Wong, M.L., and Zambryski, P. (1989). Cooperative interaction of Agrobacterium VirE2 protein with single-stranded DNA: implications for the T-DNA transfer process. Proc. Natl. Acad. Sci. USA 86: 1193-1197.
16. Citovsky, V., Zupan, J., Warnick, D., and Zambryski, P. (1992). Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256: 1802-1805.
17. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
18. Crane, Y.M., and Gelvin, S.B. (2007). RNAi-mediated gene silencing reveals involvement of Arabidopsis chromatin-related genes in Agrobacterium-mediated root transformation. Proc. Natl. Acad. Sci. USA 104: 15156-15161.
19. Das, A. (1988). Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein. Proc. Natl. Acad. Sci. USA 85: 2909-2913.
20. Day, C.D., Lee, E., Kobayashi, J., Holappa, L.D., Albert, H., and Ow, D.W. (2000). Transgene integration into the same chromosome location can produce alleles that express at a predictable level, or alleles that are differentially silenced. Genes Dev. 14: 2869-2880. (Pubitemid 30954370)
21. Doyle, J.J., and Doyle, J.L. (1990). Isolation of plant DNA from fresh tissue. Focus 12: 13-15.
22. Duckely, M., Oomen, C., Axthelm, F., Van Gelder, P., Waksman, G., and Engel, A. (2005). The VirE1VirE2 complex of Agrobacterium tumefaciens interacts with single-stranded DNA and forms channels. Mol. Microbiol. 58: 1130-1142.
23. Duckely, M., and Hohn, B. (2003). The VirE2 protein of Agrobacterium tumefaciens: The Yin and Yang of T-DNA transfer. FEMS Microbiol. Lett. 223: 1-6.
24. Dumas, F., Duckely, M., Pelczar, P., Van Gelder, P., and Hohn, B. (2001). An Agrobacterium VirE2 channel for transferred-DNA transport into plant cells. Proc. Natl. Acad. Sci. USA 98: 485-490.
25. Endo, M., Ishikawa, Y., Osakabe, K., Nakayama, S., Kaya, H., Araki, T., Shibahara, K., Abe, K., Ichikawa, H., Valentine, L., Hohn, B., and Toki, S. (2006). Increased frequency of homologous recombination and T-DNA integration in Arabidopsis CAF-1 mutants. EMBO J. 25: 5579-5590.
26. Gallagher, S.R. (1992). Quantitation of GUS activity by fluorometry. In GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression, S.R. Gallagher, ed (San Diego: Academic Press), pp. 47-59.
27. Gelvin, S.B. (2000). Agrobacterium and plant genes Involved in T-DNA transfer and integration. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 223-256.
28. Gelvin, S.B. (2003a). Agrobacterium-mediated plant transformation: The biology behind the "gene-jockeying" tool. Microbiol. Mol. Biol. Rev. 67: 16-37.
29. Gelvin, S.B. (2003b). Improving plant genetic engineering by manipulating the host. Trends Biotechnol. 21: 95-98.
30. Gelvin, S.B. (2009). Agrobacterium in the genomics age. Plant Physiol. 150: 1665-1676.
31. Gelvin, S.B., and Kim, S.-l. (2007). Effect of chromatin upon Agrobacterium T-DNA Integration and transgene expression. Blochim. Biophys. Acta 1769: 410-421.
32. Gendrel, A.-V., Lippman, Z., Yordan, C., Colot, V., and Marteinssen, R. (2002). Dependence of heterochromatlc histone H3 methylation patterns on the Arabidopsis gene DDMI. Science 297: 1871-1873. (Pubitemid 35024346)
33. Gheysen,G.,Villarroel,R.,andVanMontagu,M.(1991). lllegitimaterecombinationinplants:AmodelforT-DNAintegration.GenesDev.5:287-297. (Pubitemid21905953)
34. Gietl, C., Koukolikova-Nicola, Z., and Hohn, B. (1987). Mobilization of T-DNA from Agrobacterium to plant cells involves a protein that binds single-stranded DNA. Proc. Natl. Acad. Sci. USA 84: 9006-9010.
35. Hood, E.E., Gelvin, S.B., Melchers, L.S., and Hoekema, A. (1993). New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res. 2: 208-218.
36. Hyllus, D., Stein, C., Schnabel, K., Schiltz, E., Imhof, A., Dou, Y., Hsieh, J., and Bauer, U.M. (2007). PRMT6-medlated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev. 21: 3369-3380. (Pubitemid 350277762)
37. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
38. Jenuwein, T., and Allis, C.D. (2001). Translating the histone code. Science 293: 1064-1080.
39. Jin, C., Zang, C., Wei, G., Cui, K., Peng, W., Zhao, K., and Felsenfeld, G. (2009). H3.3/H2A.Z double variant-containing nucleosomes mark "nucleosome-free regions" of active promoters and other regulatory regions. Nat. Genet. 10.1038/ng.409.
40. Kamakaka, R.T., and Beggins, S. (2005). Histone variants: Deviants? Genes Dev. 19: 295-316.
41. Kaouass, M., Beaulieu, R., and Balicki, D. (2006). Histonefection: Novel and potent non-viral gene delivery. J. Control. Release 113: 245-254. (Pubitemid 43983040)
42. Kim SI, Veena, Gelvin SB. (2007). Genome-wide analysis of Agrobacterium T-DNA integration sites in the Arabidopsis genome generated under non-selective conditions. Plant J. 51: 779-791.
43. Kohli, A., Twyman, R.M., Abranches, R., Wegel, E., Stoger, E., and Christou, P. (2003). Transgene integration, organization and interaction in plants. Plant Mol. Biol. 52: 247-258.
44. Koncz, C., and Schell, J. (1986). The promoter of TL-DNA gene 5 controls the tissue-specific expression of chlmaeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204: 383-396.
45. Kornberg, R.D. (1977). Structure of chromatin. Annu. Rev. Biochem. 46: 931-954.
46. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128: 693-705.
47. Lacroix, B., Li, J., Tzfira, T., and Citovsky, V. (2006). Will you let me use your nucleus? How Agrobacterium gets its T-DNA expressed in the host plant cell. Can. J. Physiol. Pharmacol. 84: 333-345.
48. Lee, L.-Y., Fang, M.-J., Kuang, L.-Y., and Gelvin, S.B. (2008). Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells. Plant Methods 4:24.
49. Lee, L.-Y., Kononov, M.E., Bassuner, B., Frame, B.R., Wang, K., and Gelvin, S.B. (2007). Novel plant transformation vectors containing the superpromoter. Plant Physiol. 145: 1294-1300. (Pubitemid 350276748)
50. Li, J., Krychevsky, A., Vaidya, M., Tzfira, T., and Citovsky, V. (2005a). Uncoupling of the function of the Arabidopsis VIP1 protein in transient and stable plant genetic transformation by Agrobacterium. Proc. Natl. Acad. Sci. USA 102: 5733-5738. (Pubitemid 40559628)
51. Li, J., Vaidya, M., White, C., Vainstein, A., Citovsky, V., and Tzfira, T. (2005b). Involvement of KU80 in T-DNA integration in plant cells. Proc. Natl. Acad. Sci. USA 102: 19231-19236.
52. Li, X., et al. (2008). High-resolution mapping of epigenetic modification of the rice genome uncovers interplay between DNA methylaton, histone methylation, and gene expression. Plant Cell 20: 259-276.
53. Loidl, P. (2004). A plant dialect of the histone language. Trends Plant Sei. 9: 84-90.
54. Loyter, A., Rosenbluh, J., Zakai, N., Li, J., Kozlovsky, S.V., Tzfira, T., and Citovsky, V. (2005). The plant VirE2 interacting protein 1. A molecular link between the Agrobacterium T-eomplex and the host cell chromatin? Plant Physiol. 138: 1318-1321.
55. Luger, K., Armin, W., Mader, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. 1997 Crystal structure of the nucleosome core particle at 2.8 A° resolution. Nature 389: 251-260. (Pubitemid 27406632)
56. Luger, K., and Richmond, T. (1998). DNA binding within the nucleosome core. Curr. Opin. Struct. Biol. 8: 33-40.
57. March-Diaz, R., Garcia-Dominguez, M., Lozano-Juste, J., Leon, J., Florencio, F.J., and Reyes, J.C. (2008). Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J. 53: 475-487. (Pubitemid 351172024)
58. Marino-Ramirez, L., Kann, M.G., Shoemaker, B.A., and Landsman, D. (2005). Histone structure and nucleosome stability. Expert Rev. Proteomics 2: 719-729.
59. Matsumoto, S., Ito, Y., Hosoi, T., Takahashi, Y., and Machida, Y. (1990). Integration of chromosome: Possible involvement of DNA homology between T-DNA and plant DNA. Mol. Gen. Genet. 224: 289-302.
60. Mayerhofer,R.,Koncz-Kalman,Z.,Nawrath,C.,Bakkeren,G.,Crameri,A.,Angelis, K.,Redei,G.P.,Schell,J.,Hohn,B.,andKoncz,C.(1991).T-DNAintegration: Amodeofillegitimaterecombinationinplants.EMBOJ.10:697-704.(Pubitemid21905525)
61. Mulhausser, P., Muller, E.C., Otto, A., and Kutay, U. (2001). Multiple pathways contribute to nuclear import of core histones. EMBO Rep. 2: 690-696. (Pubitemid 32798711)
62. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15: 473-475.
63. Mysore, K.S., Bassuner, B., Deng, X.-B., Darbinian, N.S., Motchoulski, A., Ream, W., and Gelvin, S.B. (1998). Role of the Agrobacterium tumefaciens VirD2 protein in T-DNA transfer and integration. Mol. Plant Microbe Interact. 11: 668-683.
64. Mysore, K.S., Kumar, C.T., and Gelvin, S.B. (2000b). Arabidopsis ecotypes and mutants that are recalcitrant to Agrobacterium root transformation are susceptible to germ-line transformation. Plant J. 21:9-16.
65. Mysore, K.S., Nam, J., and Gelvin, S.B. (2000a). An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration. Proc. Natl. Acad. Sci. USA 97: 948-953.
66. Nam, J., Mysore, K.S., Zheng, C., Knue, M., Matthysse, A.G., and Gelvin, S.B. (1999). Identification of T-DNA tagged Arabidopsis mutants that are resistant to Agrobacterium transformation. Mol. Gen. Genet. 261: 429-438.
67. Narasimhulu, S.B., Deng, X.-B., Sarria, R., and Gelvin, S.B. (1996). Early transcription of Agrobacterium T-DNA genes in tobacco and maize. Plant Cell 8: 873-886.
68. Otten,L.,DeGreve,H.,Leemans,J.,Hain,R.,Hooykaas,P.,andSchell,J. 1984RestorationofvirulenceofvirregionmutantsofAgrobacteriumtumefaciensstrainB6S 3byconfectionwithnormalandmutantAgrobacteriumstrains.Mol.Gen.Genet.195:159-163. (Pubitemid14094160)
69. Palter, K.B., Foe, V.E., and Alberts, B.M. (1979). Evidence for the formation of nucleosome-like histone complexes on single-stranded DNA. Cell 18: 451-467.
70. Parra, M.A., and Wyrick, J.J. (2007). Regulation of gene transcription by the histone H2A N-terminal domain. Mol. Cell. Biol. 27: 7641-7648.
71. Pei, Y., Niu, L., Lu, F., Liu, C., Zhai, J., Kong, X., and Cao, X. 2007 Mutations in the Type II protein arginine methyltransferase AtPRMT5 result in pleiotropic developmental defects in Arabidopsis. Plant Physiol. 144: 1913-1923. (Pubitemid 47258114)
72. Peterson, C., and Laniel, M.A. (2004). Histone and histone modification. Curr. Biol. 14: 546-551.
73. Puebla, I., Esseghir, S., Mortlock, A., Brown, A., Crisanti, A., and Low, W. (2003). A recombinant H1 histone-based system for efficient delivery of nucleic acids. J. Biotechnol. 105: 215-226. (Pubitemid 37315764)
74. Raisner, R.M., and Madhani, H.D. (2006). Patterning chromatin: form and function for H2A.Z variant nueleosomes. Curr. Opin. Genet. Dev. 16: 119-124.
75. Ren, Q., and Govorsky, M.A. (2003). The nonessential H2A N-terminal tall can function as an essential charge patch on the H2A.Z variant N-terminal tail. Mol. Cell. Biol. 23: 2778-2789.
76. Restrepo, M.A., Freed, D.D., and Carrington, J.C. (1990). Nuclear transport of plant potyviral proteins. Plant Cell 10: 987-998.
77. Rossi, L., Hohn, B., and Tinland, B. (1996). Integration of complete transferred DNA units is dependent on the activity of virulence E2protein of Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 93: 126-130.
78. Schlaeger, E.J., and Knippers, R. (1979). DNA-histone interaction in the vicinity of replication points. Nucleic Acids Res. 6: 645-656.
79. Schrammeijer, B., den Dulk-Ras, A., Vergunst, A.C., Jacome, E.J., and Hooykaas, P.J.J. (2003). Analysis of Vir protein translocation from Agrobacterum tumefaciens using Saccharomyces cerevisiae as a model: Evidence for transport of a novel effector protein VirE3. Nucleic Acids Res. 31: 860-868.
80. Schrammeijer, B., Risseeuw, E., Pansegrau, Q., Regensburg-Tuink, T.J.-G., Crosby, W.L., and Hooykaas, P.J.J. (2001). Interaction of the virulence protein VirF of Agrobacterium tumefaciens with plant homolog of the yeast Skp1 protein. Curr. Biol. 11: 258-262.
81. Shahbazian, M.D., and Grunstein, M. (2007). Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76: 75-100.
82. Shilatifard, A. (2006). Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annu. Rev. Biochem. 75: 243-269.
83. Stachel, S.E., and Nester, E.W. (1986). The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens. EMBO J. 5: 1445-1454.
84. Stahl, L.E., Jacobs, A., and Binns, A.N. (1998). The conjugal intermediate of plasmid RSF1010 inhibits Agrobacterium tumefaciens virulence and VirB-dependent export of VirE2. J. Bacteriol. 180: 3933-3939.
85. Stewart, C.L., Roux, K.J., and Burke, B. (2007). Blurring the boundary: The nuclear envelope extends Its reach. Science 318: 1408-1412.
86. Strahl, B.D., Briggs, S.D., Brame, C.J., Caldwell, J.A., Koh, S.S., Ma, H., Cook, R.G., Shabanowitz, J., Hunt, D.F., Stallcup, M.R., and Allis, C.D. (2001). Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol. 11: 996-1000.
87. Talbert, P.B., Masuelli, R., Tyagi, A.P., Comai, L., and Henikoff, S. (2002). Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14: 1053-1066.
88. Tinland, B. (1996). The integration of T-DNA into plant genomes. Trends Plant Sci. 1: 178-184.
89. Tinland, B., Hohn, B., and Puchta, H. (1994). Agrobacterium tumefaciens transfers single-stranded transferred DNA (T-DNA) into the plant cell nucleus. Proc. Natl. Acad. Sci. USA 91: 8000-8004.
90. Tremethick, D.J. (2007). Higher-order structures of chromatin: The elusive 30 nm fiber. Cell 128: 651-654.
91. Tzfira, T., and Citovsky, V. (2000). From host recognition to T-DNA integration: The function of bacterial and plant genes in the Agrobacterium-plant cell interaction. Mol. Plant Pathol. 1: 201-212.
92. Tzfira, T., and Citovsky, V. (2002). Partners-in-lnfeetion: Host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol. 12: 121-129. (Pubitemid 34164651)
93. Tzfira, T., and Citovsky, V. (2003). The Agrobacterium plant cell interaction. Taking biology lessons from a bug. Plant Physiol. 133: 943-947.
94. Tzfira, T., Vaidya, M., and Citovsky, V. (2001). VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J. 20: 3596-3607. (Pubitemid 32634366)
95. Tzfira, T., Vaidya, M., and Citovsky, V. (2004). Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431: 87-92. (Pubitemid 39215113)
96. Verbsky, M.L., and Richards, E.J. (2001). Chromatin remodeling in plants. Curr. Opin. Plant Biol. 4: 494-500.
97. Vergunst, A.C., and Hooykaas, P.J.J. (1998). Cre/tox-medlated sitespecific integration of Agrobacterium T-DNA in Arabidopsis thaliana by transient expression of ere. Plant Mol. Biol. 38: 393-406. (Pubitemid 28443571)
98. Vergunst, A.C., Schrammeijer, B., den Dulk-Ras, A., de Vlaam, C.M. T., Regensburg-Tuink, T.J.G., and Hooykaas, P.J.J. (2000). VirB/ D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979-982.
99. Vergunst, A.C., van Lier, M.C.M., den Dulk-Ras, A., and Hooykaas, P.J.J. (2003). Recognition of the Agrobacterium tumefaciens VirE2 translocation signal by the VirB/D4 transport system does not require VirE1. Plant Physiol. 133: 978-988.
100. Vergunst, A.C., van Lier, M.C.M., den Dulk-Ras, A., Stuve, T.A.G., Ouwehand, A., and Hooykaas, P.J.J. 2005 Positive charge is an important feature of the C-terminal transport signal of the VirB/D4translocated proteins of Agrobacterium. Proe. Natl. Aead. Sci. USA 102: 832-837. (Pubitemid 40282751)
101. Wang, H., Huang, Z.Q., Xia, L., Feng, Q., Erdjument-Bromage, H., Strahl, B.D., Briggs, S.D., Allis, C.D., Wong, J., Tempst, P., and Zhang, Y. 2001 Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 293: 853-857. (Pubitemid 32743973)
102. Xiang, C., Han, P., Lutziger, I., Wang, K., and Oliver, D.J. (1999). A mini binary vector series for plant transformation. Plant Mol. Biol. 40: 711-717.
103. Yi, H., Mysore, K.S., and Gelvin, S.B. (2002). Expression of the Arabidopsis histone H2A-1 gene correlates with susceptibility to Agrobacterium transformation. Plant J. 32: 285-298.
104. Yi, H., Sardesai N, Fujinuma T, Chan CW, Veena, Gelvin SB. (2006). Constitutive expression exposes functional redundancy between the Arabidopsis histone H2A gene HTA1 and other H2A gene family members. Plant Cell 18: 1575-1589.
105. Yusibov, V.M., Steck, T.R., Gupta, V., and Gelvin, S.B. (1994). Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells. Proc. Natl. Aead. Sci. USA 91: 2994-2998.
106. Zhang, K., Sridhar, V.V., Zhu, J., Kapoor, A., and Zhu, J-K. (2005). Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS ONE 2: e1210.
107. Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S.W.-L., Chen, H., Henderson, I.R., Shinn, P., Pellegrini, M., Jacobsen, S. E., and Ecker, J.R. 2006 Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201. (Pubitemid 44380289)
108. Zhu, Y., Nam, J., Carpita, N.C., Matthysse, A.G., and Gelvin, S.B. (2003a). Agrobacterium-mediated root transformation is inhibited by mutation of an Arabidopsis cellulose synthase-like gene. Plant Physiol. 133: 1000-1010.
109. Zhu, Y., et al. (2003b). Identification of Arabidopsis rat mutants. Plant Physiol. 132: 494-505.
110. Zilberman, D., Gehring, M., Tran, R.K., Ballinger, T., and Henikoff, S. (2007). Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39: 61-69.