Expression of the Arabidopsis histone H2A-1 gene correlates with susceptibility to Agrobacterium transformation.

Transformation of plant cells by Agrobacterium tumefaciens involves both bacterial virulence proteins and host proteins. We have previously shown that the Arabidopsis thaliana gene H2A-1 (RAT5), which encodes histone H2A-1, is involved in T-DNA integration into the plant genome. Mutation of RAT5 results in a severely decreased frequency of transformation, whereas overexpression of RAT5 enhances the transformation frequency (Mysore et al., 2000b). We show here that the expression pattern of RAT5 correlates with plant root cells most susceptible to transformation. As opposed to a cyclin-GUS fusion gene whose expression is limited to meristematic tissues, the H2A-1 gene is expressed in many non-dividing cells. Under normal circumstances, the H2A-1 gene is expressed in the elongation zone of the root, the region that is most susceptible to Agrobacterium transformation. In addition, when roots are incubated on medium containing phytohormones, a concomitant shift in H2A-1 expression and transformation susceptibility to the root base is observed. Inoculation of root segments with a transfer-competent, but not a transformation-deficient Agrobacterium strain induces H2A-1 expression. Furthermore, pre-treatment of Arabidopsis root segments with phytohormones both induces H2A-1 expression and increases the frequency of Agrobacterium transformation. Our results suggest that the expression of the H2A-1 gene is both a marker for, and a predictor of, plant cells most susceptible to Agrobacterium transformation.

[1]  Spencer Brown,et al.  Characterization of competent cells and early events of Agrobacterium-mediated genetic transformation in Arabidopsis thaliana , 1992, Planta.

[2]  H. Saedler,et al.  Molecular analysis of transgenic plants derived from transformations of protoplasts at various stages of the cell cycle , 1990 .

[3]  M. Caboche,et al.  Cellular Basis of Hypocotyl Growth in Arabidopsis thaliana , 1997, Plant physiology.

[4]  M. Iwabuchi,et al.  Regulation of histone gene expression during the cell cycle , 2000, Plant Molecular Biology.

[5]  K. Okada,et al.  Efficient transformation of Arabidopsis thaliana: comparison of the efficiencies with various organs, plant ecotypes and Agrobacterium strains , 1992, Plant Cell Reports.

[6]  C. Gigot,et al.  Genes encoding a histone H3.3-like variant in Arabidopsis contain intervening sequences. , 1992, Journal of molecular biology.

[7]  A. Kvarnheden,et al.  cDNA sequence and expression of an intron-containing histone H2A gene from Norway spruce, Picea abies , 1993, Plant Molecular Biology.

[8]  V. Citovsky,et al.  The Agrobacterium DNA Transfer Complex , 1997 .

[9]  M. Chilton,et al.  Fingerprints of Agrobacterium Ti plasmids. , 1978, Plasmid.

[10]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[11]  A. Hollaender,et al.  Genetic Engineering of Plants , 1983, Basic Life Sciences.

[12]  P. Christie.  Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria , 1997, Journal of bacteriology.

[13]  B. Sangwan-Norreel,et al.  Competence of Arabidopsis thaliana genotypes and mutants for Agrobacterium tumefaciens-mediated gene transfer: role of phytohormones. , 2000, Journal of experimental botany.

[14]  S. Kresovich,et al.  NUCLEAR DNA CONTENT VARIATION WITHIN THE ROSACEAE , 1992 .

[15]  S. Gelvin,et al.  Strength and tissue specificity of chimeric promoters derived from the octopine and mannopine synthase genes , 1995 .

[16]  A. Vergunst,et al.  VirB/D4-dependent protein translocation from Agrobacterium into plant cells. , 2000, Science.

[17]  T. Tzfira,et al.  Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. , 2000, Annual review of microbiology.

[18]  C. Chevalier,et al.  Endoreduplication in higher plants , 2000, Plant Molecular Biology.

[19]  G. Ditta,et al.  Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[20]  C. Koncz,et al.  The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector , 1986, Molecular and General Genetics MGG.

[21]  S. Clough,et al.  Agrobacterium Germ-Line Transformation: Transformation of Arabidopsis without Tissue Culture , 1998 .

[22]  K. Mysore,et al.  An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  S. Gelvin,et al.  Differences in susceptibility of Arabidopsis ecotypes to crown gall disease may result from a deficiency in T-DNA integration. , 1997, The Plant cell.

[24]  M. Van Montagu,et al.  Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[25]  B. Lowe,et al.  Physical, Chemical, Developmental, and Genetic Factors that Modulate the Agrobacterium-Vitis Interaction. , 1991, Plant physiology.

[26]  L. Bögre,et al.  Differential Expression of Histone H3 Gene Variants during Cell Cycle and Somatic Embryogenesis in Alfalfa. , 1992, Plant physiology.

[27]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[28]  K. Mysore,et al.  Arabidopsis ecotypes and mutants that are recalcitrant to Agrobacterium root transformation are susceptible to germ-line transformation. , 2000, The Plant journal : for cell and molecular biology.

[29]  V. Orbović,et al.  Gibberellin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl , 1999, Planta.

[30]  S. Gelvin,et al.  Multiple copies of virG enhance the transient transformation of celery, carrot and rice tissues by Agrobacterium tumefaciens , 1992, Plant Molecular Biology.

[31]  S. C. Winans,et al.  Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. , 1996, Trends in microbiology.

[32]  J. Changeux,et al.  Calcitonin gene‐related peptide elevates cyclic AMP levels in chick skeletal muscle: possible neurotrophic role for a coexisting neuronal messenger. , 1987, The EMBO journal.

[33]  K. Mysore,et al.  Agrobacterium tumefaciens transformation of the radiation hypersensitive Arabidopsis thaliana mutants uvh1 and rad5. , 1998, Molecular plant-microbe interactions : MPMI.

[34]  S. Dinesh-Kumar,et al.  Signaling in plant-microbe interactions. , 1997, Science.

[35]  T. Nakayama,et al.  Structural characteristics of two wheat histone H2A genes encoding distinct types of variants and functional differences in their promoter activity , 1997, Plant Molecular Biology.

[36]  K. Mysore,et al.  Identification of T-DNA tagged Arabidopsis mutants that are resistant to transformation by Agrobacterium , 1999, Molecular and General Genetics MGG.

[37]  D. Inzé,et al.  Developmental expression of the arabidopsis cyclin gene cyc1At. , 1994, The Plant cell.

[38]  Stanton B. Gelvin,et al.  AGROBACTERIUM AND PLANT GENES INVOLVED IN T-DNA TRANSFER AND INTEGRATION. , 2000, Annual review of plant physiology and plant molecular biology.

[39]  M. Chilton,et al.  Plasmid required for virulence of Agrobacterium tumefaciens , 1975, Journal of bacteriology.

[40]  B. Sangwan-Norreel,et al.  Factors influencing the Agrobacterium tumefaciens-mediated transformation of carrot (Daucus carota L.) , 1992, Plant Cell, Tissue and Organ Culture.

[41]  J. L. Riopel,et al.  ORIGIN, DEVELOPMENT, AND GROWTH OF DIFFERENTIATING TRICHOBLASTS IN ELODEA CANADENSIS , 1978 .

[42]  J. R. Porter.  Host range and implications of plant infection by Agrobacterium rhizogenes , 1991 .

[43]  R. Sangwan,et al.  Histology and chimeral segregation reveal cell-specific differences in the competence for shoot regeneration and Agrobacterium-mediated transformation in Kohleria internode explants , 1996, Plant Cell Reports.

[44]  S. Gelvin,et al.  Early transcription of Agrobacterium T-DNA genes in tobacco and maize. , 1996, The Plant cell.

[45]  N. Chaubet-Gigot,et al.  Tissue-dependent enhancement of transgene expression by introns of replacement histone H3 genes of Arabidopsis , 2004, Plant Molecular Biology.

[46]  L. Moore,et al.  Host specificity in the genus Agrobacterium. , 1979 .

[47]  D. Galbraith,et al.  Systemic Endopolyploidy in Arabidopsis thaliana. , 1991, Plant physiology.

[48]  H. Puchta,et al.  Efficient Agrobacterium-mediated transformation of Arabidopsis thaliana using the bar gene as selectable marker , 1995, Plant Cell Reports.

[49]  D. Dudits,et al.  Identification of three highly expressed replacement histone H3 genes of alfalfa. , 1996, DNA sequence : the journal of DNA sequencing and mapping.

[50]  R. Horsch,et al.  Transformation of Arabidopsis thaliana with Agrobacterium tumefaciens , 1986, Science.

[51]  P. Zambryski,et al.  The transfer of DNA from agrobacterium tumefaciens into plants: a feast of fundamental insights. , 2000, The Plant journal : for cell and molecular biology.

[52]  D. Inzé,et al.  Expression of CKS1At in Arabidopsis thaliana indicates a role for the protein in both the mitotic and the endoreduplication cycle , 1999, Planta.

[53]  J. Ellis,et al.  In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants , 1993 .

[54]  A. Coleman,et al.  Relationship between Endopolyploidy and Cell Size in Epidermal Tissue of Arabidopsis. , 1993, The Plant cell.

[55]  W. Orczyk,et al.  Improved efficiency for T-DNA-mediated transformation and plasmid rescue inArabidopsis thaliana , 1993, Theoretical and Applied Genetics.