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The natural genetic engineering of plants

Jean-Pierre Zryd, Institute of Ecology, University of Lausanne, Switzerland

Genetically modified organisms are obtained by the introduction of a foreign piece of DNA into their own genome. Does this process actually differ from the natural processes occurring in plants and other living organisms? According to some people, genetic engineering is a man made tool that goes against natural laws. In fact during this century scientists have discovered that nature does a lot of shuffling, rearranging and transferring genetic material in bacteria, plants and animals: that knowledge can now be used to speed up and improve the precision of classical genetics and traditional breeding.

Genetic variations

Gregor Mendel postulated, and demonstrated through clever experiments, that the "hereditary units" (units we now call genes) which determine the visible traits of an organism rearranged themselves in a random manner during the sexual reproduction process. Since the early twenties, it has been known that during the complex processes of reproduction, rearrangement of genetic material is generated by the exchange of large pieces of genetic material. Moreover, in the early thirties, Barbara McClintock discovered that during the whole life of a maize plant, and not only during the reproductive stages, genes frequently jump from one place to another inside the genome, inducing visible mutations [5, 6]. The famous Indian corn kernels, which are so beautiful with their patterns of red and yellow stripes and spots, are an example of this phenomenon. Barbara McClintock got the Nobel prize in 1983, at the age of 81, for her theory of transposable elements (jumping genes). The fact that she received the prize as late as 50 years after her first observations is due to the strong reluctance of the scientific establishment to really accept the idea of a general genome instability. We now know that transposons are present in all organisms and active all the time; a very large portion (up to 50% and more) of the genetic material present in plants and in animals is made of a special kind of transposons named retrotransposons [2]. People who are not familiar with biology tend to think that living organisms are stable and that species are here to indefinitely stay the same; but this is not the case, we are all changing, and many species are evolving very fast. There is no doubt that an efficient inbuilt system allows controlled mutations to occur within living organisms genome; scientists think that such mutations help organisms to cope with fast changing environmental conditions: a must-equipment for plants, as they cannot move to escape.

Genetic colonization

Plant biologists are lucky people. They discovered that an ubiquitous pathogenic soil bacteria, Agrobacterium tumefaciens, is able to transfer a small but important part of its genetic material to plants during the infectious process. This genetic material is transported from the bacterial cell to the plant cell nucleus and integrates in the plant genome, where it starts making its own products. The transferred genes products induce tumour cell proliferation and the production of highly nutritious metabolites which the bacteria can feed on; those events are part of a process named genetic colonization. Scientists discovered that the bacteria can be made non pathogenic (harmless) to the plant, while remaining able to transfer a piece of DNA. From then on, the exciting story began of plant genetic transformation methods and of extensive plant genetic analysis. To transform a plant with the help of Agrobacterium tumefaciens, all you have to do is to insert a selected piece of DNA between two short specific DNA border-sequences; this is enough to allow the integration of this foreign DNA in the plant genome [1]. Such an integration is random, but unique; this means that the piece of DNA can land anywhere, but only in one place. It is then up to the geneticist to check if the integration happened in a convenient place of the genome. Today, most transgenic plants are produced by this very efficient method.

The game of recombination

Adaptation processes and evolution are characteristics of life; they result from genome modifications. We, human, are here because our primate ancestors changed before us and it is almost inevitable that we will also change with time. Genome modifications are generated, among others, by shuffling elements in a process called genetic recombination. Recombination occurs under different circumstances.
1) When a piece of DNA integrates anywhere into the genome, the process is called illegitimate recombination. It is for instance what happens when transposons move or when a plant is transformed via A. tumefaciens. Almost all transgenic plants are obtained this way. Illegitimate recombination is the predominant mechanism of recombination in most organisms.
2) When a piece of DNA integrates into a precise place of the genome by recognizing a totally identical (homologous) piece of DNA, the process is called homologous recombination. Recently it has been shown that homologous recombination can be used to transform a plant by integrating a piece of foreign DNA into a precise place of the plant genome (genes targeting). So that the mechanism can take place, the foreign piece of DNA has to contain a short sequence which is totally identical to the landing site in the genome (target). As Didier Schaefer demonstrated it in our group at the University of Lausanne, this method can be efficiently applied to the moss Physcomitrella patens [4]. Making transgenic plants through homologous recombination of small and well chosen DNA stretches promises well and should before very long become a high precision genetics method making possible subtle modifications of very small and specific part of the genome, at will [3].
Homologous recombination is a natural mechanism that occurs during the production of gametes (sexual reproduction); in this case, recombination events concern large pieces of the genome; they increase the genetic diversity. While they chose the seeds for the next season, the very early cultivators have benefited from this process (without being aware of it!), and later the conventional breeding methods which have led to our main agricultural crops took also advantage of it.

Toward increased diversity

When using conventional breeding methods, the presence of a significant variability in the plant genome is a necessity. It can be achieved by different means: the natural variability present in the extensive collection of man made cultivars (traditional and indigenous agriculture) can be used, as well as crossbreeding with identified closely related wild species (botanical survey). In the twentieth century, variability have been increased by submitting plants to ionising radiations. Radiations induce mutations (small modifications inside the genes); they have also the side effect of inducing a higher level of recombination. Most of the main crops cultivars we use today are the offspring of such mutated parents.
Many plant species, potato and orange tree for instance, spontaneously propagate without sexual reproduction. Thus, propagation by taking cuttings, layering, grafting and, more recently, by in vitro cultures has been carried out. Such vegetative (non sexual) propagation methods are not as precise however as it could be expected: sometimes, the plants you get, instead of being the same as the mother plant, largely differ from it. These differences are named somaclonal variations; they result from significant modifications of the genome and can be used to produce new varieties.
Both methods, mutagenesis and the use of somaclonal variations, significantly have increased the efficiency of conventional breeding.
Recently, DNA transfer methods (as a part of genetic engineering) have been introduced, when available, into conventional breeding. With their precision and their efficiency, these new techniques make possible to control variability more safely; they are not intended to replace other parts of the breeding technology, but to complement them.

DNA transfer: high precision genetics

DNA transfer is mainly intended for adding or modifying well known and defined genes: this part of genetics could be named "high precision genetics" in comparison with the traditional methods, which use quite unpredictable recombinations of very large parts of the genome. The introduction into a rice variety of three well known genes for the synthesis of pro-vitamin A by research groups from Swiss and German Universities is a masterly example of this strategy. Such a technical achievement is of course just a part of the whole necessary work. These high-tech rice plants are now used as parent plants in a more conventional breeding programme of which aim is to introduce this valuable trait in rice cultivars that could be used in local farming conditions. Variability, whether artificial or natural, is a source of potential hazard: it can have beneficial or neutral, but sometimes detrimental, effects; each new variety has to be tested under natural conditions. The main advantage of the new genetic of recombinant DNA (GMO) is to provide us with a more precise monitoring of the breeding processes: this is a significant benefit for all agricultural systems.

Literatur

• Gelvin SB: Agrobacterium and plant genes involved in T-DNA transfer and integration [Review]. Annual Review of Plant Physiology & Plant Molecular Biology 51: 223-256 (2000).
• Kumar A, Bennetzen JL: Plant retrotransposons [Review]. Annual Review of Genetics 33: 479-532 (1999).
• Puchta H, Hohn B: From centimorgan to base pairs - Homologous recombination in plants [Review]. Trends in Plant Science 1: 340-348 (1996).
• Schaefer DG, Zryd J-P: Efficient gene targeting in the moss Physcomitrella patens. The Plant Journal 11: 1195-1206 (1997).
• Wessler SR: Transposable elements and the evolution of gene expression. [Review] [75 refs]. Symposia of the Society for Experimental Biology 51: 115-22 (1998).
• White SDJ: Of genes and genomes and the origin of maize. [Review] [32 refs]. Trends in Genetics 14: 327-32 (1998).