Historical perspectives on plant developmental biology
MIEKE VAN LIJSEBETTENS* and MARC VAN MONTAGU
Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, Gent, Belgium
*Address correspondence to: Dr. Mieke Van Lijsebettens. Department of Plant Systems Biology, VIB2-Universiteit Gent, Technologiepark 927, B-9052 Gent, Belgium. Fax 32-9-331-3809. e-mail: mieke.vanlij[email protected]
Around 1950, B. McClintock’s and P. Peterson’s analyses in maize led to the description of mobile DNA in the genome. McClintock correlated chromosome breakpoints at specific positions with mobile DNA elements, called Dissociator (Ds) and Activator (Ac), that caused specific changes in phenotypes explained by the altered expression status of known gene loci such as the C locus (McClintock, 1950). This new vision of the genome being dynamic was confirmed in bacteria, animals and other plant species. The molecular basis of mobile DNA in several plant species was demonstrated later (Fedoroff et al., 1983; Döring et al., 1984; Pohlman et al., 1984; Pereira et al., 1985). The cloning of the bronze locus in maize with the Ac transposable element was one of the first examples of «gene tagging» in plants (Fedoroff et al., 1984). Moreover, the Ac/Ds and En/Spm elements, endogenous to the monocotyledon maize, were shown to be active in the dicotyledonous tobacco (Baker et al., 1986; Masson and Fedoroff, 1989; Pereira and Saedler, 1989). These studies pioneered the use of mobile DNA in large-scale mutagenization programs of the plant genome for gene discovery. Introduction of mobile DNA into heterologous plant genomes required a transformation step that was solved by the study of the tumor-inducing (Ti) principle of the plant-colonizing bacterium, Agrobacterium tumefaciens. In 1974, it was demonstrated that a plasmid was present in oncogenic Agrobacterium strains and absent from non-oncogenic strains (Zaenen et al., 1974). It resulted in the hypothesis that this plasmid was the Ti principle and it was indeed shown that a fragment of the plasmid, the socalled T-DNA was transferred to the plant genome (Chilton et al., 1977; De Beuckeleer et al., 1978). The T-DNA contained a number of genes, the so-called oncogenes, encoding plant hormone- synthesizing enzymes that were driven by eukaryotic promoters that became active in the plant cell upon infection (Joos et al., 1983; Zambryski et al., 1989). Only the T-DNA borders and the virulence genes on the Ti plasmid were essential for T-DNA transfer and integration into the plant genome. All the T-DNA genes could be replaced by chimeric selectable marker genes or other genes and stably integrated and expressed into the plant genome (Bevan et al., 1983; Fraley et al., 1983; Zambryski et al., 1983; De Block et al., 1984; Horsch et al., 1984). The T-DNA was further engineered as a versatile vector for plant transformation and such vector construction is still ongoing today (Karimi et al., 2002). The plant transformation procedures benefited from earlier research on in vitro propagation and regeneration of explants on sterile mineral salt solutions (Murashige and Skoog, 1962) that contained different ratios of phytohormones to promote either callus, root, or shoot growth from explants (Linsmaier and Skoog, 1965). Digestion of explants to single protoplasts and subsequent regeneration into fertile plants was a great advancement because these regenerated plants were clonal (Nagata and Takebe, 1970; Nagy and Maliga, 1976; Lörz et al., 1979). The integration of the protoplast regeneration procedure with Agrobacterium infection opened the way to produce clonal transgenic cell lines in tobacco at first (Márton et al., 1979). Some plants appeared to be recalcitrant to in vitro regeneration and Agrobacterium transformation. It took more than a decade to succeed in a wide variety of plant species. Efficient Agrobacterium tumefaciens - mediated transformation methods that were tissue culturebased and accessible to the entire academic community were established for the model plants Arabidopsis thaliana, Oryza sativa and Zea mays (Valvekens et al., 1988; Hiei et al., 1994; Frame et al., 2002). In the meantime, a number of important technological breakthroughs were made in molecular biology, such as the cloning into plasmid vectors, the determination of the DNA sequence of the first viral organism (Fiers et al., 1978) and gene expression analysis (Kamalay and Goldberg, 1984). The subsequent automatization of the sequencing technology resulted in the whole genome sequence of the first flowering plant, namely that of Arabidopsis (Arabidopsis Genome Initiative, 2000). High density micro-arrays allowed for quantitative genome-wide expression analyses and contributed to the systems biology approach of biological questions (Lipshutz et al., 1999). The in vitro DNA amplification via the polymerase chain reaction (PCR) revolutionized plant biology because the large genomes were made accessible for experimentation (Mullis and Faloona, 1987). The β-glucuronidase gene of Escherichia coli was the first reporter gene adapted for use in plants (Jefferson et al., 1987) and was replaced ten years later by the green fluorescent protein (GFP) from jelly fish because of its application in living explants using confocal microscopy (Haseloff et al., 1997). A timeline is presented in Table 1.
Source: Int. J. Dev. Biol. 49: 453-465 (2005)
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