Prehistory and history of Arabidopsis research.

The earliest non-taxonomic appearance of Arabidopsis in the literature of botany appears to be a paper by Alexander Braun in 1873, describing a mutant plant found in a field near Berlin (7). The mutation was almost certainly in the AGAMOUS gene, now well known as one of the floral ABC regulators and cloned in 1990 (54). The next notable appearance of Arabidopsis in the experimental literature was in 1907, when Friedrich Laibach (1885–1967), a student in Strasburger’s laboratory in Bonn, published an account of the chromosome number of several plants. He was attempting to find a plant with a small number of large chromosomes to be used in experiments to determine the individuality of chromosomes (23). Arabidopsis was not such a plant: the chromosomes are very small. The next relevant appearance of Arabidopsis was in a 1935 paper that resulted from a Russian expedition to find a plant that could be used in genetics and cytogenetics, as Drosophila was then used (15, 51). Although the small chromosome number (incorrectly stated by Titova to be a haploid no. of three; Laibach had correctly counted five in 1907) and rapid time to flowering were considered useful features, the small size of the plant and its parts were considered a disadvantage, as was the inability to distinguish different chromosome pairs. It does not appear that Arabidopsis was ever used in the laboratory by Titova and her colleagues. Arabidopsis crops up again as a subject for laboratory investigation in 1943 when Laibach described the early results of studies in which he showed the short generation time, fecundity, ease of crosses, and the possibility of mutagenesis, and on this basis proposed adoption of Arabidopsis as a genetic model organism (24). The detailed results of the Laibach laboratory’s studies on x-ray mutagenesis, which led to the first collection of Arabidopsis mutants, were published as a Ph.D. thesis by Laibach’s student Erna Reinholz. The full publication of her 1945 thesis was, in fact, by the U.S. military: it seems that the thesis, with the word “Röntgen-Mutationen” in the title, came to the attention of those looking for a German atomic bomb program. It was published in 1947 as an unclassified captured document of the Joint Intelligence Objectives Agency (46). There are reports through the 1950s and 1960s of the creation of mutants (25) and mutant collections (34, 35), of methods for generation of embryo lethals, and use of such methods to assess mutagenicity of chemicals (40, 44), and of use of the plant for controlled-environment studies and quantitative genetics (26, 27), but surprisingly little use was made of what is now such a central organism for laboratory work on flowering plants. There were the first stirrings of organization: A newsletter called Arabidopsis Information Service was founded in 1964 (publication continued until 1990). The original advisory board was F. Laibach, A. Müller, G. Rédei, and J. Veleminsky, with G. Röbbelen of the University of Göttingen serving as editor. Starting with the 1974 issue, the position of editor was taken by Albert Kranz of the University of Frankfurt. Two International Congresses of Arabidopsis were held before the molecular biology era: the first in Göttingen in April, 1965 (Fig. 1) and the second in Frankfurt am Main in September of 1976 (Fig. 2). Laibach and his students continued their Arabidopsis work by collecting a large number of ecotypes, which after their organization by Albert Kranz, formed the basis for the current ecotype collection (22). The widespread adoption of Arabidopsis as a model plant, followed by the current revolution in plant genetics, physiology, and molecular genetics, occurred in the 1980s (Fig. 3). The idea that plant biologists should concentrate on a model organism was then under intense discussion, and a number of proposals were made such as using petunia because of its ease of transformation and the availability of haploid lines, or using tomato because of the availability of mutants (e.g. 42). Use of Arabidopsis for genetic experiments in plant physiology, in particular for finding auxotrophic mutations, had been proposed by George Rédei in 1975, in an article in the Annual Review of Genetics that brought Arabidopsis to the attention of many young geneticists and soonto-be molecular cloners (45). What swung the balance in favor of Arabidopsis is not certain, though several contributions can be pointed out. One was the demonstration that mutational analysis can be done to saturation in laboratory conditions, and therefore that informative mutations in any gene could be obtained in screens of a practicable size (48, 49). Another was the demonstration that Arabidopsis has a very small genome and is therefore convenient for gene cloning, which at that time was difficult for large-genome organisms (28, 43); yet another was * E-mail [email protected]; fax 626 – 449 – 0756.