Saturday, October 18, 2014

Haberlandt’s Dogmatic Dream and Its First Realisation

As vividly described in the review by Vasil (2008), the alleged friendship between the botanist Matthias Jakob Schleiden (1804–1881) and the animal physiologist Theodor Schwann (1810–1882) stimulated, among others, the formation of the “cell theory”. Schleiden (1838) was the first to formulate the hypothesis that all plant or animal structures are composed of cells (or their derivatives) that preserve the complete functional potential of the organism.


Half a century after the cell theory had been formulated, both plant and animal biologists started to verify it experimentally. Initially, attempts were made to demonstrate the “immortality” of animal and plant somatic cells by means of their in vitro culture. The next challenge – only successful for plants – was to regenerate functionally complete organisms from these cultured tissues.

Against the preconceived expectation that the high functional autonomy of autotrophic plant cells would make it easier to cultivate them in vitro, it was an “animal” researcher who won the first round of this race when Ross Granville Harrison, working at Johns Hopkins Medical School and later at Yale University, published his results of experiments from 1907 to 1910, which established the methodology of animal tissue culture (Harrison 1907). It took a further quarter of a century before comparable results were achieved for plants, by the independent work of White (1939), No ´becourt (1939) and Gautheret (1939).

The possible reasons for Haberlandt’s persistent failure to persuade isolated plant cells to divide in vitro have been extensively discussed in various critical reviews. Maybe the most objective conclusion is that reached by Gautheret (1985): Unfortunately, he (Haberlandt) was influenced by Schleiden and Schwann’s cell theory rather than by experimental expectation. And he neglected both Duhamel’s results as well as Vo ¨chting’s and Rechinger’s experiments (Note: experiments with plant parts containing various meristematic tissues, thus generating calli or regenerating buds; cf. Gautheret). His dogmatic attitude and the ignorance of the past explain the failure of his own attempts. But he appreciated very clearly that, when the technical difficulties were removed, the method of cultivating isolated cells in nutrient solution should make possible the experimental study of many outstanding problems from a new point of view. He, therefore, chose to work with single cells. Appreciating the importance of photosynthesis he presumed that green cells would be the best material. However, he neglected the fact that green cells of phanerogams are relatively differentiated and cannot recover meristematic competence without stimulating substances which were unknown at the time. He worked with palisade cells of Lamium purpureum, pith cells from petioles of Eichhornia crassipes, glandular hairs of Pulmonaria and Urtica, stamen hairs of Tradescantia, stomatal guard cells of Ornithogalum, and many other materials.

At this time it was recognized that asepsis was absolutely necessary when culture media were enriched in organic substances metabolized by microorganisms. Haberlandt’s media contained glucose and peptone, he carefully avoided contamination and his cultures remained free of microorganisms. The results, however, were disappointing. The cells survived for several weeks. They were capable of synthesizing starch and enlarging, but they were never dividing. Fifty six years passed before the realization of Haberlandt’s dogmatic dream....

Undoubtedly, it was mainly thanks to the use of these phytohormones that Muir et al. (1954, 1958) succeeded in obtaining new cell colonies from isolated cells of Nicotiana tabacum and Tagetes erecta. Application of a synthetic auxin, 2,4-dichlorophenoxyacetic acid (2,4-D), in the culture medium allowed Steward et al. (1966) not only to obtain a well-growing suspension culture of carrot callus cells and their aggregates but also to regenerate from them somatic embryos of potentially unicellular origin. Eventually, as a result of the long-term competition between the Skoog and Steward teams to isolate and identify the active compound in the plant “fetal serum”, i.e. coconut milk (for a review, see Amasino 2005), cytokinins were first isolated and became a universal component of the plant tissue culture media. Vimla Vasil and Hildebrandt (1965a, b) convincingly documented the whole procedure “from a somatic cell to a regenerated plant” by means of time-lapse photography of individual cells of the hybrid Nicotiana glutinosa ? Nicotiana tabacum. From a recovered single-cell-based colony, they regenerated the entire flowering plants, exploiting the results by Skoog and Miller (1957) on the influence of auxin to cytokinin ratio on regeneration.

These experiments, however, failed to prove the validity of Haberlandt’s vision “from individual somatic cells to complete plants”; the problem was that the primary explants used were multicellular and thus the original callus colonies from which the so-called single-cell clones were derived. Later technology, how-ever, finally confirmed Haberlandt’s original dream in all its details. It was shown that when single cells were stripped of their cell walls to produce the so-called protoplasts (Cocking 1960, 1972, 2000; Takebe et al. 1971), these protoplasts were able to regenerate not only into walled cells (Nagata and Takebe 1970; Opatrny ´et al. 1975, 1980) but also into complete plants (Takebe et al. 1971; Schumann et al. 1980). Isolated protoplasts, cultured separately in microchambers, could regenerate real “protoclonal plants”.

Through the alternative methodology of pollen culture, developed in the late 1970s, new (even haploid) plant organisms can be generated directly from plant spores.

But, in spite of these discoveries, experimental knowledge remained limited by the mostly empirical approach to regeneration. Moreover, the use of regenerative techniques in both fundamental research and practical applications repeatedly encountered the problem of “recalcitrance” of a particular model material. This recalcitrance depended either on species, variety or genotype; the origin of cuttings or explants used; the age or composition of the material; and a variety of other features. As a rule, further detailed studies on the factors affecting plant developmental and regenerative abilities and mechanisms were – and still are – necessary to solve such problems.

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