Rapid evolution of defense genes in plants may produce hybrid incompatibility

July 08, 2007

One of the basic tenets of evolution is speciation in which populations of the same species become so genetically and morphologically variable that they can be classified as two different species. Individuals of these species may be capable of mating, but they may not produce offspring, and if offspring are produced, they will be sterile or so defective that they die before they are able to reproduce. Although speciation has been observed and studied since Darwin and Wallace first proposed their theory, the complex molecular mechanisms responsible are not yet fully known. One of these molecular mechanisms, hybrid necrosis, was studied by Dr. Detlef Weigel and his colleagues at the Max Planck Institute for Developmental Biology in Germany. Dr. Kirsten Bomblies will present their results at the President's symposium at the annual meeting of the American Society of Plant Biologists (July 11, 2PM). Bomblies and Weigel observed hybrid necrosis in crosses of thale cress, Arabidopsis thaliana, a member of the mustard family, and found that it is associated with plant genes that respond to pathogen attack.

Plants must frequently cope with environmental stresses such as heat, cold, high acidity or salinity, or attack by pathogens such as viruses or insect predators. Such stresses mobilize defense genes that initiate physiological responses that help the plants to survive. One such response is programmed cell death, which occurs in response to invasion by viruses or bacteria. The cells invaded by the pathogens are quickly marked by the plant for death so that the microbe cannot use them to replicate and spread to the rest of the plant. These types of genes have been shown to evolve rapidly, giving plants the capability to adapt to changing conditions and pathogens. Bomblies and Weigel found that the same type of gene is involved in hybrid incompatibility in Arabidopsis. Because these genes evolve so rapidly, there are likely to be different forms present in the population, and when two of these are joined in a hybrid, they can cause fatal defects in the hybrid offspring.

A biological species is defined as a population of individuals that can interbreed among each other freely, but not with members of other species. What finally establishes two populations as different species is that gene flow between them stops. However, this does not happen suddenly. Rather, it is a gradual process in which one barrier after another is raised between two species, including inviable embryos and defective and sterile adults, as well as genetic incompatibilities that prevent even the formation of an embryo. The hybrid incompatibility identified by Bomblies and Weigel is an example of the kind of genetic incompatibility that can result in speciation.

Because plant reproduction often requires an outside agent like a pollinator or the wind, which spreads pollen far from the parent plant, the offspring can be hybrids between parents from two different populations or even from two different although closely related species. Such hybrid offspring can be successful but may also be prevented or defective because some of the parents' genes are not compatible. In their survey of 900 first generation hybrid offspring among 293 strains of thale cress, Bomblies and Detlef found that 2% of the offspring were severely defective. They call this phenomenon "hybrid necrosis" or "hybrid weakness," and identified the gene responsible for the incompatibility as a disease resistance gene that has different forms in the two parents.

Some of the molecular mechanisms that prevent hybridization between species are well-known in both animals and plants. There are a number of gene flow barriers in plants that are similar to those of animals--among them are ecological factors such as reproductive season, morphological differences, and hybrid sterility. However, hybrid necrosis produced by autoimmune responses due to pathogen resistance genes has not been observed in animals and may represent a molecular pathway to speciation unique to plants. Knowledge of these mechanisms is important not only in the study of the evolutionary history of plants but can also provide tools for ensuring the safety of genetically engineered crops. If incompatibility genes can be bred into a GE crop, it might be possible to prevent the formation of superweeds and to lessen the probability that harmful genes can be spread to other species.
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American Society of Plant Biologists

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